28
Chapter 17 Adaptation, Acclimation and Regulation in Algal Photosynthesis John A. Raven* Division of Environmental and Applied Biology, School of Life Sciences, University of Dundee, Dundee 001 4HN, U.«. Richard J. Geider Department of Biological Sciences, University of Essex, Colchester C04 3SQ, U,«. Summary 386 I. Introduction 386 II. The Range of Resource Availabilities and Other Environmental Factors within Which Algae Can Photosynthesize 389 III. Adaptation of the Photosynthetic Apparatus 390 A. Background 390 B. Light Harvesting 390 C. Photosynthetic Electron Transfer Chain 391 D. Photoprotection and Xanthophyll Cycle Pigments 393 E. Ribulose Bisphosphate Carboxylase/Oxygenase 394 F. (Phospho)glycolate Metabolism 395 G. Enzymes Involved in Protection from Photooxidative Stress 395 V. Adaptation of Algal Photosynthesis to Environmental Extremes 396 A. Light 396 B. Inorganic Carbon Supply 398 C. pH 399 D. Oxygen Concentration 399 E. Temperature 400 F. Pressure 400 VI. Acclimation of Algal Photosynthesis 400 VII. Regulation of Algal Photosynthesis 406 VIII. Rates of Regulation and Acclimation 407 IX. Conclusions 408 Acknowledgments 409 References 409 *Author for correspondence, email: [email protected] Anthony W. Larkum, Susan E. Douglas and John A. Raven (eds): Photosynthesis in Algae, pp. 385-412. © 200j Kluwer Academic Publishers.

[Advances in Photosynthesis and Respiration] Photosynthesis in Algae Volume 14 || Adaptation, Acclimation and Regulation in Algal Photosynthesis

  • Upload
    john-a

  • View
    213

  • Download
    0

Embed Size (px)

Citation preview

Chapter 17

Adaptation, Acclimation and Regulation inAlgal Photosynthesis

John A. Raven*Division of Environmental and Applied Biology, School of Life Sciences,

University of Dundee, Dundee 001 4HN, U.«.

Richard J. GeiderDepartment of Biological Sciences, University of Essex, Colchester C04 3SQ, U,«.

Summary 386I. Introduction 386II. The Range of Resource Availabilities and Other Environmental Factors within Which Algae

Can Photosynthesize 389III. Adaptation of the Photosynthetic Apparatus 390

A. Background 390B. Light Harvesting 390C. Photosynthetic Electron Transfer Chain 391D. Photoprotection and Xanthophyll Cycle Pigments 393E. Ribulose Bisphosphate Carboxylase/Oxygenase 394F. (Phospho)glycolate Metabolism 395G. Enzymes Involved in Protection from Photooxidative Stress 395

V. Adaptation of Algal Photosynthesis to Environmental Extremes 396A. Light 396B. Inorganic Carbon Supply 398C. pH 399D. Oxygen Concentration 399E. Temperature 400F. Pressure 400

VI. Acclimation of Algal Photosynthesis 400VII. Regulation of Algal Photosynthesis 406VIII. Rates of Regulation and Acclimation 407IX. Conclusions 408Acknowledgments 409References 409

*Author for correspondence, email: [email protected]

Anthony W. Larkum, Susan E. Douglas and John A. Raven (eds): Photosynthesis in Algae, pp. 385-412.© 200j Kluwer Academic Publishers.

386

Summary

John A. Raven and Richard J. Geider

Relating the photosynthetic processes of algae to their environments requires that the responses are consideredover time-scales of seconds to minutes (regulation), hours to days (acclimation) and up to thousands ofmillionsof years (adaptation). All of these responses are genetically determined, with so-called adaptations reflectinggenetic changes which distinguish taxa from the strain (ecotype), i.e. infraspecific level, up to the Division(Phylum) level. Tempting as it is to assign the establishment ofthese genetie differences to natural selection, thegenetic differences at the higher taxonomic levels should be related to the environments at the time at which theyevolved. Genetic differences limit the responses that algal genotypes can make to their immediate environment(i.e. during a single generation). Using photosynthetic pigments as an example, the content per unit biomass ofphotosynthetic light-harvesting pigment-protein complexes, and, where they occur, of the energy-dissipatingxanthophyll cycle pigments change with the photon flux density for growth; light-harvesting pigments decreasewith increasing light, while xanthophyll cycle pigments increase. There are cost-benefit considerations not onlyin the extent ofsuch acclimation, but also ofthe rate at which acclimation occurs. Regulation involves allostericor covalent modification ofpre-existing catalysts, e.g. ribulose bisphosphate carboxylase-oxygenase, xanthophyllcycle pigments, and the pigment-protein complexes involved in state transitions. Much remains to be done tonot only understand adaptation, acclimation and regulation in algae, but also to understand how the threeprocesses interact.

I. Introduction

Algal photosynthesis proceeds according to the(minimal) equation)

catalysts

CO2 + 2H2*0 + 8 photons ~ (CHP) + *02 +Hp

The adaptation and acclimation of the photo-synthetic machinery in algae concerns the responsesof the organisms to variability in the availability ofthe substrates (C02, Hp and photons), and variabilityin the build-up ofthe produets (02 and (CHP)), ofphotosynthesis. It also concerns variability of theavailability of the resources that are required to

Abbreviations: CAM - Crassulaccan acid metabolism; cro-Cf'. - chloroplast or cyanobacterial ATP synthetase; dd-dt -diadinoxanthin-diatoxanthin cycle; I - incident photon fluxdensity; Tk - saturation function of photosynthesis; photon fluxdensity at which the extrapolation of the initial slope of thephotosynthesis.incident photon flux density relationship intcrectsthe extrapolation of the light-saturated rate of photosynthesis;Km -- Michaclis-Mcnten constant; L,- form II Rubisco with twolarge subunits; L,S, - form I Rubiseo with eight large and eightsmall subunits; NADH - nicotinamide adenine dinucleotide(reduced form); NADP+ - nicotinamide adenine dinucleotidephosphate (oxidized form); PQ - plastoquinone; PQ'- - plasto-semiquinone; PQH,-plastoquinol; PS 1- Photosystcm 1;PS IIPhotosystem IT; '1',- pressure component of water potential; 'l'n-osmotic component of water potential; \T~, - water potential;RCIT- reaction center of Photosystem 11; Rubisco - ribulosebisphosphate carboxylase-oxygenase; UQ - ubiquinone; UQ'--ubi semiquinone; UQTI, - ubiquinol; v-a-z - violaxanthin-antheraxanthin-zeaxanthin cycle

produce the catalysts used in the photosyntheticreactions. Among these requirements for producingthe catalytic apparatus of photosynthesis are thecarbohydrates produced by photosynthesis, and thenutrients obtained from the environment. Thesenutrients include N (immediately as NH;), P (asIIPOl-), Mg21, Cl-, Mn21, Fe2-/Fe3+, Zn" and (often)Cu2+. The availability of these resources in algalhabitats varies widely, in some cases by at least fourorders ofmagnitude (Table 1).At the outset we need to differentiate clearly

amongst the terms adaptation, acclimation and regu-lation' . Adaptation will be used to describe an out-come of evolution as reeorded in the gene pool of aspecies. It also refers to changes in gene frequencywithin a gene pool as a result of selection with orwithout recombination. Acclimation will be used todescribe changes ofthe macromolecular compositionofan organism that occurs in response to variation ofenvironmental conditions. According to this usage,photoacclimation occurs via synthesis or breakdownof specific components of the photosynthetic appar-atus. Acclimation operates within constraints set bythe genetic make-up of the species (or, more often,the clonal population) under investigation. Regulation

1 The term adaptation has been employed loosely in studies ofalgal photosynthesis and ecology to refer to genetic adaptation,physiological acclimation and physiological regulation. We feelthat it is necessary to differentiate between these processes. Theterm behavior can be reserved for activities such as swimming orother movements/migrations.

Tab

le1.Rangeofexternalconditionsinwhichatleastsomealgaecangrowphotolithotrophically.Naturalconditionsunlessotherwisespecified.

o zr Ol "0 Cii

..... --.,J

Environmentalfactor

Minimumvalueatwhichphotolithotrophic

Maximumvalueatwhichphotolithotrophic

References

growthcanoccur

growthcanoccur

20nmolphotonm-2s-1(crustosecoralline

::>2mmolphotonm?S-1(fullsunlight)

marineredalgagrowingat274m)

AslittleasI,umolphotonm-2S-1fordeep-

Usuallyatleast0.5,umolphotonm-2S-1

watercrustosecorallineredalga

Photon/luxdensityof

photosyntheticallyactive

radiation400-700nm

UV-Bfluxdensity280-320nm

Inorganiccarbonconcentration

CO2concentration

pI!

02concentration

Temperature

Waterpotential('¥w)

components

'¥pand'¥-:

'¥w='¥p~'¥n

o Immolm-3(?)insome

Immolm-3(?)insome

0.5

(Dun

alie

lla

acid

ophi

la)

1.0(Cyanidiophyceae)

-0(laboratory)

-1.8°C(cyanobacteria,eukaryotesin

Antarctic)

-38MPa('¥n)

(Dun

alie

llainDeadSea;

Apa

toco

ccusontreetrunks)

'¥p+0.1MPa:atmosphericpressureatsea

level;higherinDeadSea,lowerathigh

altitudes)

~ 100molm"(cyanobacteriainsodalakes)

Lowerforsomeotheralgae

2::80mmolm:'

(Cya

nidi

umco

ldar

iums.l.

invitro)

::>30molm-3

(Chl

orel

lainvitro)

II(somecyanobacteria,Chlorophyta)

::>Irnolmf

(Ent

erom

orph

a,U

lva)

Lowerforsomeotheralgae

+45°C(Cyanidiophyceae)

+55°C(cyanobacteria)

+2.84MPa('¥p)(crustosccorallinemarine

redalgagrowingat274m,withatmospheric

pressureof+0.1MPaatthesurfaceadded

to2.74MPadueto274mdepthofwater)

('¥n-

2.46

:seawater)

+I.MPa('¥p)(benthicalgaegrowingat

150minLakeTahoe,withatmospheric

pressureofMPaatthesurfaceaddedto

1.50MPadueto150mofwater

'¥rr-0.005MPa;verylowosmoloarity

freshwater)

Raven,KiiblerandBcardall(2000)

FranklinandForster(1997)

Raven(1990)

Raven(1990)

Raven(1990)

Ravenetal.(1994)

RavenandGeider(1988)

Raven(I984a,1993),Raven,

KublerandBeardall(2000)

» 0- Ol "0 ~ o' ::J ~ Q.

~r ~ o' ::J Ol ::J 0- J) CD (Q c ?I o'

::J w 00 -.l

388

will be used to describe the adjustments of catalyticefficiency that occur without net synthesis orbreakdown ofmacromolecules. Adaptation, acclima-tion and regulation are generally thought to actaccording to rules that optimize performance(maximize evolutionary success or fitness) withinconstraints set by the environmental conditions. Inphotosynthesis optimization involves a trade-offamong:

• maximizing the rate of photosynthesis per unitof resource (energy, carbon, nitrogen, etc. used)in constructing the photosynthetic apparatus.

• maximizing the quantity ofCO2 fixedper incidentphoton when light is limiting photosynthesis,and

• minimizing the damage that can arise from excesslight, UV radiation, and oxygen radicals.

Regulation operates on a time scale of seconds tominutes. Acclimation operates on a time scale ofhours to days. Adaptation operates on a wide rangeoftime scales from days for shifts in gene frequency,to seasons or years for species replacement duringsuccession, to hundreds of millions of years for theevolution of new species. Together, the processes ofadaptation, acclimation and regulation determinethe niche that a population occupies. Adaptationrefers to the hard-wired genetic information withinan organism, whereas acclimation and regulationrefer to the implementation ofthis information withinspecific environmental contexts.The genetic basis for photosynthesis by algae

sensu lato involves thousands of (morphologicallydefined) species ofCyanobacteria, and of the tens ofthousands of species of species of algal eukaryotesderived from them and a protist host by endosym-bioses (Chapter 1, Douglas et al. and Chapter 2,Larkum and Vesk).These include primary endosym-biosis ofa cyanobacterium-like ancestor to producethe Chlorophyta and Rhodophyta (and Glaucocysto-phyta), and secondary endosymbiosis of photo-synthetic eukaryotic cells to yield the Euglenophytaand Chlorarachniophyta (endosymbiosis of a greenalga) and the Heterokontophyta, Haptophyta,Cryptophyta and (probably) Dinophyta (endo-symbiosis ofa red alga). This diversification ofalgaeinvolves not only the evolution ofthe Cyanobacteria

John A. Raven and Richard J. Geider

and the plastids which arc derived from ancestralCyanobacteria, but also the genetic variability in thechemoorganotrophic 'host' eukaryotes. This involvesseven chemoorganotrophic eukaryotic taxa as thehosts for the photosynthetically active symbiontswhich ultimately became the plastids that we knowtoday (van den Hoek et al., 1995; Chapter 1,Douglaset al.). This genetic 'mixing and matching' in theevolution of the algae provides the basis forevol utionary adaptation of algae to particularphotosynthetic environments.The occurrence of tens of thousands of species of

algae sensu lato implies, via classic niche theory, theoccurrence of a corresponding number of nicheswhich may not, of course, all relate directly orindirectly to photosynthetic reactions. However, G.E. Hutchinson has pointed out that there are moremorphologically defined species of phytoplanktonalgae than there arc obvious niches. This isHutchinson's 'paradox ofthe plankton', and it can beapplied to algal habitats other than the plankton (aswell as to many animal habitats). One way round thisparadox is the involvement of more environmental(biotic and abiotic) factors in the definition ofnichesthan have previously been used. These include thequantitative use of factors in the form of resourceavailability ratios and clone-specific or speeies-specific disease (viruses, protista and fungi) and/orgrazing pressure. A further means of resolving theparadox is to invoke temporal variability in thehabitats such that competitive exclusion of one (ormore) species by another species that is better adaptedto that habitat does not go to completion before thecombination of environmental conditions changesand alters the selective balance. Such 'explanations'become even more necessary as molecular geneticmethods and redefinitions of the criteria formorphologically defined species (e.g. of diatoms),increase the number of species (or ecotypes) to beaccommodated in the niches.Complementary to adaptation is acclimation, i.e.

phenotypic changes in an organism within ageneration and without any genetic change con-trasting with adaptation which involves geneticchange over a number of generations. Acclimationincreases the niche width for a given genotype. Theoccurrence of so many species of algae shows thatacclimation has significant constraints. Presumablythe constraints on the extent of acclimation involvethe greater fitness of a genotype when growing in a

Chapter 17 Adaptation, Acclimation and Regulation 389

habitat close to its optimum than when acclimated toa very different habitat. In other words, there aregenotypes ofother species that have greater fitness inthis environment that is far from optimal for ouracclimating species.Acclimation operates within the genetic constraints

set by adaptation. Although not yet available for anyalga sensu stricto (i.e. a non-em bryophyte eukaryoticphototroph), complete nucleotide sequences ofgenomes should be very useful in examining thelimits ofacclimation within genotypes. Not all genesare expressed simultaneously. Thus, complete genesequences will show the range of traits that can beexhibited by the genotype. Complete nucleotidesequences for the cyanobacterium Synechocystis sp.PCC 6803 (Kaneko et al., 1996) and other Cyano-bacteria (Hess et al., 2001) are proving very helpfulin probing adaptation and acclimation, especially ifthe constitutive or inducible nature of the enzymes(or other proteins) encoded can be determined. A(non-algal) example of the complete genomesequence of an organism that can tolerate veryextreme conditions (by the standards of the majorityoforganisms) isDeinococcus radiodurans Rl (Whiteet al., 1999). This gram-positive non-photosyntheticbacterium has the greatest resistance to ionizingradiation of any known organism, as well as greattolerance of UV-B radiation and desiccation. Thefirst two attributes (and possible the third) relate tothe very wide range of DNA repair mechanismsavailable, often with multiple gene copies, and the 5-10 copies ofthe genome in growing cells. Resistanceto ionizing radiation also correlates with desiccationtolerance in Cyanobacteria (Potts, 1999). Again, theextent to which the mechanisms are constitutivelyexpressed and the extent to which some of them areinducible deserves exploration.This chapter deals with adaptation, acclimation

and regulation as they relate to algal photosynthesis.We shall see that the outcomes of adaptation and ofacclimation to particular environments are frequentlysimilar, presumably as a result of constraints due tophysics and chemistry and to evolutionary history.Before considering adaptation and acclimation, weconsider the range of environments in which thephotosynthetic apparatus can function, takingphotosynthetic algae as a whole.

II. The Range of Resource Availabilities andOther Environmental Factors within WhichAlgae Can Photosynthesize

Table I summarizes the range ofresource availabilitiesand other environmental factors which are consistentwith photosynthetic growth of extant algae. Of thefactors which can be expressed as ratios ofmaximumto minimum values, the ratio for photosyntheticallyactive radiation is at least 105, for inorganic carbonthe concentration ratio is 105, for CO2 the concen-tration ratio is almost lOS, while for (external) H~activity the ratio is 101°.Some of the extremes of the ranges of environ-

mental factors in Table I, e.g. the 80 mmol rrr' CO2tolerated by growing Cyanidium may seem laboratoryartifacts, irrelevant to the present environments inwhich algae grow, while others (photon flux density,pH, 02) do reflect environments inwhich algal growthoccurs today. However, even the extremely high CO2levels tolerated by Cyanidium have natural parallelsin the past. Thus, the Earth's atmosphere at the timeof the evolution of photosynthesis (3.5-3.8 millionyears ago) probably had CO2 partial pressure ofseveral atmospheres (i.e. a significant fraction of IMPa) (Falkowski and Raven, 1997; Cockell, 2000),with a decreasing trend (but with significantvariations) subsequently; ocean pH would corres-pondingly have been lower than the present value atearlier times. 02 was at about 10-8 of the presentatmospheric level, i.e. at the partial pressure generatedby atmospheric photochemistry, until just before 2billion years ago when global accumulation ofphotosynthetically produced 02 began (Falkowskiand Raven, 1997), with an increasing trend (but withsignificant variations) subsequently. Solar energyoutput has increased, as has the maximumwavelengthand total energy of solar emission, over the 4.5billion years of the Earth's existence (Falkowski andRaven, 1997). The increase in photosyntheticallyactive radiation over the last 4.5 billion years is some25%, while the flux ofUV-B radiation has decreased(Falkowski and Raven, 1997). The current (Pleis-tocene) glaciations are an exception to the generaloccurrence of a warmer Earth with smaller equatorto pole temperature gradients, so sea surface waterscooler than 5°C or so have been the exception duringthe time that algae have existed (Falkowski andRaven, 1997).Extant algae have a day of 24 h and a year of 365

390

days. With increasing latitude the photoperiod showsincreasing seasonal variation. The phasing ofcellularactivities to the diel cycle of light and darknessrelates to circadian rhythms as reset by light (andtemperature) cycles. In strongly seasonal environ-ments a number ofmacroalgae arc 'seasonal antici-pators' (Kain, 1989), i.e. change their behavior in amannerwhich relates to the 'expected' environmentalconditions in the following weeks or months. Thiseffect is probably related to circadian rhythms(Luning, 1993). While the length of the year has notchanged over the time (~3.8 billion years) for whichlife has existed on earth, the daylength has almostdoubled and the number of days per year has almosthalved as the lunar orbit has receded from the Earthwith retention of angular momentum (Walker et al.,1983), so presumably circadian rhythms have almostdoubled their free-running periods. Without the moonthe Earth's obliquity would not have been stabilizedat 23.3° ± 1.3" (Laskar et al., 1993), and the resultingchaotic variations in obliquity would have hadprofound photoperiodic consequences (Cockell,2000).

III. Adaptation of the PhotosyntheticApparatus

A. Background

Some ofthe putative adaptations ofthe photosyntheticmachinery concern the occurrence of differentcatalysts or ratio of catalysts of particular reactionsamong taxa. The processes that will be consideredare (1) light-harvesting pigments and associatedproteins, (2) substitutions within the photosyntheticelectron transport chain, (3) xanthophyll cyclepigments, (4) state transitions, (5) variations in themain carboxylating enzyme, ribulose bisphosphatecarboxylase/oxygenase (Rubisco), (6) enzymesinvolved in glycolate metabolism and (7) enzymesinvolved in protection from photo-oxidative stress.

B. Light Harvesting

The rate of light absorption sets an upper limit onalgal productivity. There arc large differences in lightabsorption spectra, as well as in the distribution ofexcitation energy between Photosystems I and II,among the higher alga taxa (Fig. I; see also Chapter13, Larkum).

John A. Raven and Richard J. Geider

We can consider here the occurrence of at leastfour types of light-harvesting pigment-proteincomplexes (for a full description refer to Chapter 13,Larkum). These are the (1) phycobilin complexes,(2) chlorophyll a/b complexes, (3) fucoxanthin-chlorophyll complexes and (4) peridinin-chlorophyllcomplexes, although we note that each of these fourtypes of complexes may have arisen more than oncein the evolution of the algae. Phycobilin light-harvesting pigment-protein complexes occur to theexclusion of chlorophyll-based complexes in mostCyanobacteria and red algae. Other algae havechlorophyll-based complexes instead of, or as wellas, the phycobilins (Rowan, 1989; Larkum and Howe,1997; Raven, 1998, 1999; Raven et al., 2000; Table 2).The 02-evolvers with only phycobilins as tetrapyrrole-based light-harvesting pigments other than chloro-phyll a have higher ratios of PS I to PS II than doother 02-evolvers (Falkowski and Raven, 1997;Larkum and Howe, 1997; Raven et al., 1999;Table 1).The occurrence of structurally and spectrally

different light-harvesting complexes in differenthigher taxa ofalgae led Engelmann (1883) to attemptto relate the zonation of higher taxa of intertidal andsubtidal seaweeds on rocky shores to their pigmen-tation via the different light climates in which thevarious algal taxa grow. This insightful suggestionby Engelmann (1883) has been validly criticized onseveral grounds, e.g. the great variation in spectraltransmission ofcoastal seawaters, the general absenceofa 'green-brown-red' sequence of algal zones withincreasing depth, and the high absorptance ofmanymacroalgal thalli which via a large package effect,minimizes the differences in absorption as a functionofwavelength among higher taxa of algae (Crossettet al., 1965; Larkum et al., 1967; Dring, 1981, 1982;Raven, 1984a,b; Kirk, 1994).Engelmann's (1883) hypothesis could apply to

optically thin algal structures, e.g. unicells and theyoung stages ofmacroalgae (Raven, I984a,b, 1986,1996, 1998, 1999). For the phytoplankton there issome relationship between habitat and geneticallyconstrained pigmentation but there are severalcounter-examples (Raven, 1996, 1998, 1999).Verticalmixing (Maclntyre et al., 2000) over variable depths,which can be tens ofmeters, will clearly complicateany relationship of light climate and pigmentation.As for the young, relatively low absorptance, stagesof macroalgae, Harvey (1836) was prescient inpointing out that coloration (as a taxonomic criterion)was best seen in reproductive stages (spores, gametes)

Chapter 17 Adaptation, Acclimation and Regulation 39 1

700600

P.minimum

500

8 r-- - - - - - - - ---,

700

C.muelleri

600500O '----~-------"

400

4I::a

2:a...a afIl.0 6«...aQ)oI::Q)o

2fIlQ)...a:::lu:::Q)

.~ E. hux/eyiroQ)0::

Wave length (nm)

Fig. 1. Absorption (solid lines) and fluorescence excitation (dotted lines) spectra forthe diatom Chaetoceros muelleri, the dinoflagellateProrocentrum minimum, the chlorophyte Dunaliella tertiolecta, the cryptomonad Chromonas salina, the prymnesiophyte Emilianiahuxley i and the cyanobacte rium Synechococcus. Spectra are normalized such that the areas under both the absorption and fluorescencespectra are equal. Fluorescence emission was measured at 730 nm, and arises primarily from Photosystem II.The filled area between thecurves indicates the spectral region in which excitation energy is preferentially delivered to Photosystem II. In other regions of thespectrum , excitation energy is preferentially delivered to Photosystem I. The largest mismatch between absorption and fluorescenceexcitation spectra is for the cyanobacterium. Figure provided by Dr. David Suggett.

of seaweeds and freshwater macrophytes. However,attempts to interpret (a la Engelmann, 1883) theestablishment of macroalgae in terms of theirpigmentation and light quality,while not falling foulof high absorptance, still cann ot explain fully theobserved zonation patterns in terms of the (variable)spec tra l quality of incident radiation at a given depthin coas tal seawater (Raven et a1., 2000 ; Raven andKubler, 2002 ).The earliest members of the higher taxa of algae

(Divis ion, Class) were prob ably unicellul ar and oflow absorptance. Thus, the spectral diversity of theirpigments could have influenced pho tosynth eticperformance at low incident irradi ances, providedthat the cells were disper sed rather than aggragatedin a mat (Raven, 1996, 1999). Even so, it is not easyto relate the spectral differences in light-harvestingpigment s among higher taxa of algae with the

environment in which they presumably evolved, e.g.deep in the water column as a response to the higherUV-B output of the sun early in the Earth's history(Raven, 1996 , 1999; Falkowski and Raven, 1997).

C. Photosynthetic Electron Transfer Chain

There are two locations in the photosynthetic electrontransfer chain where markedly different catalystsperform similar functions. The se are between thecytochrome bJ complex and PS I where plasto-cyanin and cytochrome c6 serve as electron carriersand downstream of PS I where flavodoxin cansubstitute for ferredoxin . Red algae and those derivedby secondary endosymbiosis of red algal cells andeuglenoids have only Cytochrome c6• Other algae(Cyanobacteria,Chlorophyta) have only plastocyaninor both plastocyanin and cytochrome c6 (a point

Tab

le2.Genotypic('adaptive')variationinphotosyntheticcharacteristicsamongalgae

ICyanobacteriasensustricto;2Cyanobacteriawithchlorophylldareassignedtothe

gcnu

sAca

ryoc

hlor

is;3Somccyanobacteriadesignatedashavingchlorophyllbactuallyuscdivinyl

chlorophyll

b;"ClassesofIIetcrokontophytaaredesignatedasfollows:b~Bacillariophyceae;c=Chrysophyceae;e=Eustigmatophyccae;p=Phaeophyceae;x=Xanthophyceae;

5Xanthophyllcyclecomponentsaredesignatedasfollows:a=antheraxanthin;dd=diadinoxanthin;dt=diatoxanthin;v=violaxanthin;z~zeaxanthin;6PCOC=Photorespiratory

CarbonOxidationCyele;References:Badgeretal.(1998);FalkowskiandRaven(1997);Gossetal.(1998);LarkumandHowe(1997);LohrandWilhelm(1999);Raven(1987,1988,

1997,1999);Ravenctal.(1989,1999,2000);Rowan(1989);andsectext.

LowCO2affinity,Moderate-high

ModerateCO2

LowCO2

ModerateCO2

?low

C0

2/0

2CO2affinity,

affinity,highto

affinity,low

affinity,

selectivity

moderate-high

veryhigh

CO

i02

moderate

CO

i02

C0

2/0

2selectivity

CO

i02

selectivity

selectivity

selectivity

Characteristics

Photosynthetic

light-harvesting

pigments

Redoxcatalyst

forelectron

transferfrom

cytochrome

bJ'

toPSI

Occurrenceof

statetransitions

Occurrenceof

xanthophyll

cycle"

Rubisco

characteristics

Glycolate

metabolism(b)

Cyanobacteria

Chlorophylla+

phycobilinsI(or

chlorophyll

a+

phycobilins+

chlorophyll

bor

d2 ,orchlorophyll

a+chlorophyll

b3

(±chlorophyllc-

likepigments)

Plastocyanin

and/or

cytochromec6

Present

Absent

Glycolate

dehydrogenase;

partialPCOC

Chlorophyta

Chlorophyll

a+

chlorophyll

chlorophyllc-

likepigment)

Plastocyanin

and/or

cytochromec6

Present

Usuallypresent

(v-a-zorv-a)

Glycolate

dehydrogenase

(allexcept

Charophyceae);

glycolateoxidase

(Charophyceae);

PCOC

Cryptophyta

Chlorophyll

a+

ehlorophyllsc+

phyeobilins(in

thylakoidlumen,

not

phycobilisomes)

Cytochromec 6

(?)

Probablyabsent

Absent

Glycolate

dehydrogenase,

then?

Dinophyta

Chlorophyll

a+

chlorophyllc2+

peridinin(orlike

almostevery

otheralgal

Divisionasa

resultof

secondary

endosymbiosis)

CytochromeC6

Absent?

Present(dd-dt,

-'-v-a-z)

Glycolate

dehydrogenase,

then?

Euglenophyta

Chlorophyll

a+

chlorophyll

b

Cytochrome

Present?

Present(dd-dt)

Glycolate

dehydrogenase;

modifiedPCOC

Haptophyta

Chlorophyll

a+chlorophylls

c-fucoxanthin

andderivatives

CytochromeC6

(?)

Absent?

Present(dd-dt;

+v-a-z)

Glycolate

dehydrogenase?

then?

Hetcrokontophyta

chlorophyll

chlorophyll,c+

fucoxanthin

(b,c,p,x);

chlorophyll

a+

violaxanthin(c)

Cytochromec6

Absentorlow

amplitude

Present(dd-dt+

v-a-zinb,c;

v-a-zinp,x)

ModerateCO2

affinity,highto

veryhigh

CO

i02

selectivity

Glycolateoxidase;

PCOC(p);glycolate

oxidase;malate

synthase(x);

glycolate

dehydrogenase,

malatesynthase(b);

glycolateoxidase,

then?

Rhodophyta

chlorophyll

a+phycobilin

±chlorophyll

d

Cytochromec6

Present

Absent

Moderateto

highCO2

affinity;highto

extremelyhigh

CO

i02

selectivity

Glycolate

oxidase;

PCOC

W '0 tv c.... a ::J'":::J » ::D OJ < CD :::J OJ :::J

Q.. ::D o· ::J'"

OJ .... Q.. c....G)

CD 0: CD ....

Chapter 17 Adaptation, Acclimation and Regulation 393

which will be considered later under acclimation)(Table 2) (see Raven et al., 1999, and Hope, 2000, fora discussion of kinetic comparisons of piastocyaninand cytochrome c6) .

There are considerable variations in the capacityfor the Fe-containing ferredoxin to be replaced bythe Fe-free flavodoxin among marine microalgae,and f1avodoxin has been reported to be constitutivein some species (Geider and La Roche, 1994). Thereis a general correlation between the habitat oforiginof a genotype and its capacity to produce f1avodoxinunder low-Fe culture conditions. La Roche et al.(1995) found that flavodoxin expression was inducedby iron-limitation in all nine species ofmarine diatomsexamined, including the oceanic isolate Thalassiosiraoceanica. Erdner et al. (1999) examined 17 speciesfrom four classes of algae, and found no capacity toproduce flavodoxin in one ofthree dinophytes and inthe only cyanobacterium tested. Three of the fivespecies which could not produce f1avodoxin werefrom coastal (i.e. generally Fe-rich) habitats; onewas of unknown origin, while the cyanobacteriumSynechococcus sp. was from the Fe-poor SargassoSea and thus is a counter-example (Erdner et al.,1999). Another counter example is the ferredoxin-free (flavodoxin only) red macroalga Chondrus fromcoastal waters (Raven et al., 1999).

O. Photoprotection and Xanthophyll CyclePigments

Genetic differences among higher taxa of algae canalso be seen in two traits related to photosyntheticlight harvesting and photoprotection. These are statetransitions and the occurrence of the xanthophyllcycle as ameans ofnon-photochemical quenching ofexcitation energy (Lohr and Wilhelm, 1999;Maclntyre et al., 2000; Chapter 13, Larkum).State transitions involve changes in the association

of light-harvesting complexes with reaction centersas a function ofthe total irradiance, and the spectraldistribution of photosynthetically active radiation(Chapter 13, Larkum). State transitions are known inthe phycobilosome-eontaining Cyanobacteria andred algae, most green algae and in higher plants, butare apparently absent or small in chromophytes sensulato (Raven et al., 1989; Fork et al., 1991; Larkumand Howe, 1997; Finazzi et al., 1999; MacIntyre etal., 2000). The variations in excitation energy transferto the two sorts of reaction center can occur rapidly,i.e. over time intervals resembling those ofvariationsin light-climate of the understory of a kelp forest,

and may help to limit photodamage to D1protein inPS II by limiting excitation energy transfer to PS Il athigh irradiances (Falkowski and Raven, 1997;Table 2). It is not easy to see ecological advantages inthe qualitative or quantitative differences in statetransitions among the various phyla and classes ofalgae. It is possible that the occurrence and extent ofstate transitions relates to the difference in absorptionspectra between the pigments which supply excitationenergy to PS II and those which service PS 1.Thus,state transitions are well developed in Cyanobacteria(sensu stricto, with phycobilin) and Rhodophyta,and are absent or minimal in 'chromophytes ' (e.g.Heterokontophyta): Table 2.Xanthophyll cycles are involved in non-photo-

chemical excitation energy quenching. The twocharacterized xanthophyll cycles involve de-epoxi-dation of violaxanthin to antheraxanthin andultimately zeaxanthin (v-a-z) or de-epoxidation ofdiadinoxanthin to diatoxanthin (dd-dt). Zeaxanthinand diatoxanthin are the quenching, de-epoxidizedforms of the xanthophylls, and violaxanthin anddiadinoxanthin are the non-quenching forms. The v-a-z cycle occurs inmembers ofthe Chlorophyta (andEmbryophyta), and the Eustigmatophyceae, Phaeo-phyceae and Chrysophyceae in the Heterokontophyta,although some green algae seem to lack a xanthophyllcycle (Rowan, 1989; Demmig-Adarns and Adams,1992; Franklin ct al., 1996; Franklin and Larkum,1997; Lohr andWilhelm, 1999; Chapter 13,Larkum).In Mantoniella there is a reduced cycle where onlythe v-a interconversion occurs. The dd-dt cycle occursin the Dinophyta, Euglenophyta, Haptophyta and inthe Bacillariophyceae and Xanthophyceae in theHeterokontophyta, although in the cases examinedthere is a subsidiary v-a-z cycle in organisms withthe dd-dt cycle (Rowan, 1989; Lohr and Williams,1999). Despite the use of the v-a-z cycle in bothgreen algae and embryophytes, the latter have moremechanistic similarities of their xanthophyll cyclewith those algae predominantly using the dd-dt cycle(MacIntyre et aI., 2000).Notable absentees from the list above are the

Cyanobacteria, the glaucocystophytes and therhodophytes (Table 2). No data seem to be availablefor the glaucocystophytes. For Cyanobacteria andrhodophytes most data indicate the absence of axanthophyll cycle (Table 2), although Ursi et al.(2003) present evidence consistent with the presenceof a v-a-z cycle in the red alga Gracilaria birdae.Furthermore, Subramanian et al. (1999) found areversible covalent change in photosynthetic

394

chromophores in the marine cyanobacteriumTrichodesmium which, like the covalent changes inthe xanthophyll cycles, reduced excitation energytransfer to PS II reaction centers at high incidentphoton flux densities. In Trichodesmium the covalentchange involves the conversion ofphycoerythrobilin(with efficient excitation energy transfer to PS IIreaction centers) to phycourobilin (with substantialfluorescent loss of the light it absorbs) as lightincreases and vice versa as light decreases(Subramaniam et aI., 1999). While it is not yetknown ifthis phenomenon in Trichodesmium involvesprotein phosphorylation (as do state transitions) it isclear that it does involve covalent modification ofphotosynthetic chromophores (as do xanthophyllcycles).MacIntyre et al. (2000) note that Cyanobacteria,

which lack a xanthophyll cycle (but see above), havea very significantMehler reaction activity (02 uptakeby the reducing end ofPS I) at light saturation (Kana,1992). This can act as a sink for electrons when PS IIactivity exceeds net photosynthetic capacity. Diatomsmay use non-assimilatory nitrate reduction as anelectron sink (Lomas and Glibert, 1999), supple-menting whatever Mehler reaction activity occurs(Bunt, 1965). Franklin and Badger (200 1) haveprovided important data on the extent of Mehlerreaction activity in marine macroalgae.In view of the wide ecological range of the higher

taxa of organisms with the light harvesting, redoxcatalyst, state transition and xanthophyll cyclecharacteristics and the great ecological overlapbetween taxa with differing traits described above, itis difficult to perceive the traits which characterizethe various phyla and classes of algae as beingadaptations to very specific habitats, even when theglobal environment at the time at which the traitevolved is considered (Raven 1984a; Falkowski andRaven, 1997; Raven etal., 1999,2000). Furtherworkon the mechanism ofexcitation energy quenching bydc-cpoxidized components of the xanthophyllcycle( s) may show whether the presence of phyco-bilisomes on the outer thylakoid membrane surfaceas major light-harvesters for PS II is incompatiblewith non-photochemical quenching in the xanthophyllcycle(s) at the inner side ofthe thylakoid membrane.

E. Ribulose Bisphosphate Carboxylase/Oxygenase

There are very significant variations at the Class and

John A. Raven and Richard J. Geider

Division levels in the kinetics of carboxylation andoxygenation by Rubisco (Table 2). One line ofevolution of Rubisco starts with the cyanobacterialLsSs (i.e. with eight large and eight small subunits)enzyme with a low CO2 affinity and low CO/02selectivity, and a high maximum specific reactionrate ofcarboxylation at CO2 saturation. This Rubiscoclade is retained in the plastids of green algae,euglenoids, chlorarachniophytes and higher plants,where the CO2 affinity and CO/02 selectivity arehigher, and the CO2-saturated carboxylation rate islower, than in the cyanobacterial enzyme (Table 2).These traits are especially pronounced in Rubiscoswhich function with diffusive supply ofCO 2 (e.g. inthe lichen alga Coccomyxa: Raven et aI., 2000). Theyare less pronounced, or suppressed entirely, whenCO2 is supplied to Rubisco by a CO2 concentratingmechanism (Raven et a!., 2000).A second line of Rubisco evolution occurs in

prokaryotes as an LsSs form in j3-proteobacteria (i.e.organisms related to the ancestors ofmitochondria).Lateral gene transfer has incorporated this variant ofRubisco into some Cyanobacteria, and into red algaeand hence into all plastids derived from them bysecondary endosymbiosis (Raven et aI., 2000). Inthese Rubiscos the CO/02 selectivity is higher thanthe cyanobacterial line of Rubiseos, with very highvalues (three times the highest value in thecyanobacterial line) in some thermophilic andacidophilic red algae (Raven et a!., 2000; Table 2). Inall of these cases oflateral gene transfer the original(cyanobacterial) Rubisco has been displaced. Theglaucocystophytes, which like red and green algaeare the result of the primary endosymbiotic eventwhich gave rise to plastids, resemble red algae inlacking chlorophyll b and having phycobilins, butresemble green algae in the form of LsSs Rubiscothat they contain (Badger et al., 2002).Lateral gene transfer is also involved inthe presence

of L2 (two large subunits) Rubisco in peridinin-containing dinoflagellates. This form of Rubiscooriginated in j3-proteobacteria, and has a very lowCO2 affinity and CO/02 selectivity (Table 2; Ravenet al., 2000).The diversity ofkinetics ofRubis co has significant

impacts on the energy requirements for the netconversion ofCO2 to carbohydrate in photosynthesis(Raven, 2000; Raven et a!., 2000) for the defaultcondition ofdiffusion ofCO2 from an air-equilibriumsolution as the means of supply of CO2 to Rubisco,and with the photorespiratory carbon oxidation cycle

Chapter 17 Adaptation, Acclimation and Regulation 395

as the means ofmetabolizing phosphoglycolate (seebelow). Attempts to relate i) the genetic variation inRubisco kinetics to the habitat occupied by theorganisms today, ii) the occurrence of carbonconcentrating mechanisms and iii) the inorganic Csupply conditions when the various phyla and classesof algae evolved, have only met with partial success(Raven, 1997,2000; Raven et aI., 2000).

F (Phospho)glycolate Metabolism

Significantphosphoglycolate production via Rubiscooxygenase activity occurs for photosyntheticorganisms with diffusive supply ofCO2from an air-equilibrium solution even when the Rubisco involvedhas the highest known CO/02 selectivity value(Raven et a!., 2000; Table 2; Chapter 8, Beardall etal.). All algae, including those Cyanobacteria whoseCO2concentrating mechanism maintains a very highCO2level around Rubisco, have a phosphog1ycolatephosphatase and a glycolate oxidase and/or dehydro-genase, as well as some enzyme(s) metabolizingglyoxy1ate(Table 2; Raven etal., 2000). The diversityofpathways ofglycolate metabolism in algae (Table2) cannot readily be accounted as adaptive in termsof the present habitats of the organisms and thehabitat at the time at which the algal taxon originated(Raven, 1997,2000; Raven et a!., 2000).

G. Enzymes Involved in Protection fromPhotooxidative Stress

The enzymes involved with the removal of activeoxygen species generated (predominantly) by photo-synthetic processes include superoxide disrnutases,ascorbate and glutathione peroxidases, and catalase(Raven et aI., 1999). These enzymes show significanttaxonomic diversity within the algae, especially withrespect to the different superoxide dismutases withtheir various metal ion requirements (Fe, Mn, Cu +Zn) and the capacity among eukaryotes to express anSe-containing glutathione peroxidase as well as anFe-containing ascorbate peroxidase (Chadd et a!.,1996; Raven et al., 1999).Earlier, less complete data sets allowed some

workers to make plausible correlations ofthe timingof the availability of metals and the origin of taxawith superoxide dismutases containing these metals,and especially the late origin of the green algal classCharophyceae when the free 02 build-up made Cuavailable. However, later data, including the

occurrence of Cu-Zn superoxide dismutase in acyanobacterium and the early occurrence of otherCu-containing catalysts such as cytochrome oxidaseand plastocyanin, make such historical adaptationarguments less plausible (Chadd et aI., 1996; Ravenet aI., 1999), even allowing for the possibility oflateral gene transfer. Clearly the enzymes, togetherwith the scavengers and quenchers, which removeactive oxygen species evolved very early in the historyof photosynthetic O2 evolution, where, even withsignificant inorganic reductants available as 02 sinks,there was local O2 build-up (Canfield and Teske,1996; Bjerrum and Canfield, 2002). These enzymes,scavengers and quenchers are the adaptive responseto the qualitative presence of 02 above the minimal(l0-8 of the present atmospheric level) amountproducedphotochemically in the atmosphere. Clearlyin an anoxygenic world, oxygen was a very dangerouschemical which had to be detoxified quickly.However,as with several of the enzyme systems discussedabove, it is not easy to see adaptation in most of thecurrent phylogenetic or environmental distributionof these enzymes. Perhaps these events took placemuch too early to have any phylogenetic significancein the modern world.At lower taxonomic levels (genera, species,

varieties) wemight expect more recent environmentalconstraints to act as agents of natural selection thanin the consideration ofthe characteristics ofdivisions(phyla) or classes.An important point which should be considered in

any analysis of possible selective advantages ofputative adaptations is that a given trait may servemore than one selective end, and thus be acted on byseveral environmental factors. This may especiallybe the case for morphological traits. Thus, organismsize among phytoplankton organisms impacts onefficiency (per pigment molecule) of the absorptionof radiation, nutrient (including inorganic C) avail-ability, sinking/flagellar motility, and susceptibilityto grazing (Raven, 1998, 1999). In Phaeocystis spp.(Haptophyta) there is an alternation between uni-cellular zoospores (3 .urn) and millimeter-size colonies(Moison and Mitchell, 1999). Despite a negativeimpact on the effectiveness of light and nutrientabsorption, the colonial form is frequently favored,probably in relation to immunity from grazing bysome herbivores (Moison and Mitchell, 1999; Plouget a!., 1999a,b).

396 John A. Raven and Richard J. Geider

V. Adaptation of Algal Photosynthesis toEnvironmental Extremes

A. Light

Dealing firstwith the availability oflight, the classicalsuite of ,sun' and 'shade' adaptations found in studiesofhigher land plants by Bjorkman (1981 )and othershave significantly influenced views of algal adap-tations to extremes ofphotosynthetically active radi-

ation. in addition to newer constructions as to howthe photosynthetic reactions at low photon flux den-sities can be seen as outcomes of mechanismsfostering the avoidance ofphotodamage as well as ofmeans whereby the organism maximizes photon useat low photon flux densities (Osmond and Grace,1995), there are a number of algal responses whichare not entirely in accord with the higher plant 'sun!shade' paradigm. However, the general adaptiveresponse in algae seems to involve larger photo-

Light-Saturated Rate Initial Slope

0.0 2.0 4.0 6.0 0.00 0.02 0.04

0 00

F 0 0

20 20 0

0 0

40 0 40 0

0

60 0 60 0

0 0

80· 0 80 0

0

100 100 0

0120 0 120 0

140 140

Light Saturation

0 200 400

00

H 020 0

040 0

060 0

080 0

0100 0

0120 0

140

O.OE

o

G

Chlorophyll a Cell Abundance

0.00 0.20 0.40 0.0 0.5 1.0

0 00

C D ~..--o~~020 0 20

0

~~40

0 40

060 0 60

080 80

0 .s-:100

0 100

0120 120

0

140 140

8

Nitrateo 2 3 4 5

o e---'---"--~~---j

20

40

60

80r-,100

120

140

Percent Surface Light

0 50 100

0

A20

40g..c 60tsOJ0 80

100

120

140

Cell Fluorescence0.0 0.5 1.0

0

E20·

40gs: 60c..OJ ,0 80 ·i

100

120 o.......~~

140

Fig. 2. Vertical profiles of environmental and biological variables for the oligotrophic North Atlantic Ocean. A) Attenuation ofphotosynthetically active radiation. B) Nitrate concentration (,umol I-I) showing low values in surface waters and a pronounced nitriclinebelow 90 m. C) Chlorophyll a concentration (pg I-I). D) Relative abundance ofSynechococcus spp. (open circles) and Prochlorococcusspp. (filled circles). Abundance is expressed as a percentage of the maximum value observed for each taxon. E) Relative cell-specificfluorescence arising from chlorophyll a for Synechococcus spp. (open circles) and Prochlorococcus spp. (filled circles). Fluorescence isexpressed as a percentage of the maximum value observed for each taxon. F) The light-saturated photosynthesis rate (units of g C[gChI a] I h 1 of the phytoplankton assemblage. G) The light-limited initial slope of the photosynthesis-light response curve for the entirephytoplankton assemblage (units of g C m2 s [g ChI a /lIllol photons h]'. H) The light saturation parameter for the entire phytoplanktonassemblage (units of /lIllol photons m- 2 S-I). Observations of light, nitrate, cell abundance and cell-specific fluorescence were providedby Marcel Veldhuis (Netherlands Institute ofSea Research). The parameters of the photosynthesis-irradianee response curve were takenfrom Bouman et al, (2000).

Chapter 17 Adaptation, Acclimation and Regulation 397

synthetic units (total light harvesting pigment perPS I or PS II reaction center) in the shade-adaptedplants.Whether photoadaptation contributes significantly

to the success of a species in nature has not beendetermined, although among the marine picophyto-plankton, there is a tendency for the smaller divinylchlorophyll a plus b-containing Prochlorococcus tolive at greater depths than the larger chlorophyll aplus phycobilin-containing Synechococcus (Fig. 2).This may be related to the absorption maxima of thepigments ofProchlorococcus which are particularlyappropriate for harvesting blue-green radiation deepin clear oceanic waters, and the smaller packageeffect in the smallerProchlorococcus cells and hencethe more rapid payback oflight energy investment inpigments in a given light field in Prochlorococcusthan in Synechococcus (Raven, 1984b, 1998, 1999;Bricaud et al., 1999; Ting et al., 2002). Furthermore,the depth distribution of Prochlorococcus clones isconsistent with genetic adaptation to high- or low-irradiance environments (Moore and Chisholm, 1999;Hess et al., 2001). Specifically, Prochlorococcusclones with higher chlorophyll b/a ratios, higherlight-limited growth rates and greater susceptibilityto photoinhibition are found deeper in the watercolumn. In the subsurface chlorophyll a maximumlayer in the Sargasso Sea, Prochlorococcus sp. hadgrowth rates that were twice those ofthe co-occurringphytoplankton (Goericke andRepeta, 1983;Goerickeand Welschmeyer, 1993). However, it must beacknowledged that the deepest-growing benthic algae(Littler et al., 1985; Littler and Littler, 1994; Ravenet al., 2000) are red crustose corallines with a largeabsorptance. In addition, these algae employ light-harvesting pigments with a high energy-cost in theirproduction per unit light absorption rate in a givenelectromagnetic radiation environment (Raven,1984a,b).The depth distribution of Synechococcus and

Prochlorococcus ecotypes may not be attributedexclusively to the marked light gradient. Verticalstratification is also evident in profiles, with nutrient-depleted waters of the surface mixed layer overlyingthe nutrient-replete waters below the thermocline.Given the nitrogen-limited condition ofthe waters inwhich Synechococcus is commonly found (Grazianoet al., 1994) and the high nitrogen costs ofphycobiliprotein synthesis, it is somewhat surprisingto find Synechococcus as the most abundantphotosynthetic organism in the oligotrophic North

Atlantic. Parts of the ocean are Fe-deficient, and Fedeficiency induces the production ofnovel chlorophylla-containing light-harvesting supercomplexes (lsiA)in Synechococcus (Boekema et aI., 2001; Bibby etal., 200 Ia) which permit photosynthesis to occurwith fewer Fe-rich PS I units with larger antennacomplexes (Raven et al., 1999). The large PS I-isiAunits in Fe-deficient Synechococcus arc evolutionarilyrelated to such units in Prochlorococcus (Bibby etaI.,200Ib).In this section we consider the absolute constraints

on growth at the extremes of high and low photonflux density at which algae can grow.The upper limitof photon flux density for growth may be set byphoto inhibitory damage (Osmond and Grace, 1995;Forster et al., 2001). Current perception is that damageto the D1polypeptide is caused by one in every 106 to107 of absorbed photons which arrives at photo-reaction two reaction centers (Franklin and Larkum,1997; Raven et al., 2000; Chapter 16, Franklin et aI.).Restriction ofthis damage in high light environmentsinvolves a small photosynthetic unit size, sometimesaccompanied by the ability to dissociate some lightharvesting apparatus from the PS II reaction centers.It also involves mechanisms whereby non-photo-chemical quenching is increased, as well as regulatoryand behavioral mechanisms which restrict photonabsorption overall (see above). The extent to whichthese mechanisms occur is phylogenetically variable.Thus, Cyanobacteria and red algae cannot vary theextent of non-photochemical quenching via axanthophyll cycle. Both ofthe avoidance mechanismswhich restrict the extent of photodamage, albeit atthe expense of the short-term photosyntheticpotential, themselves are regulated, i.e. highirradiances lead to the dissociation oflight harvestingcomplexes from reaction center two, and to thedepoxidation of epoxycarotenoids to producequenching carotenoids (see below). This must bedistinguished from acclimation (considered below),in which the extent to which the underlying mechan-isms are expressed alters in response to rather longertime scales, but still in response to environmentalchanges which are short-term relative to the timescale of several to many generations required foradaptation. Of course, the mechanisms that limitphotodamage by varying the fraction of absorbedphotons which reach photoreaction two centers areonly necessary to the extent that photon flux densityvaries. Adaptation to continuous very high photonflux densities would only require a small photosyn-

398

thetic size to minimize the potential for photodamagewhile permitting maximal productive use of incidentphotons in photosynthesis at the high irradiancc.Even with such aminimal photon harvesting capacitythere might be constraints on effective photon use,with the possibility of spatial mis-match of the sitesof primary photochemistry and of the catalysts ofdownstream reactions. However, there are precedentsfor photosynthesis without detectable photoinhibitionat a very high incident photon flux density (Forster etaI., 200 I), even up to 3000 J1ITIol photon rrr ' S-1 in adinoflagellate symbiont in a coral (Falkowski andDubinsky, 1980; Long et aI., 1994).Thus the potentialfor photodamage, presumably inherited from theearliest 02-evolvers, can be dealt with in some algaeand permit photosynthesis at one and a halftimes themaximal natural photon flux density of 2000 J1ITIolphoton m-2 S-I.At the other end ofthe scale we have algae growing

at very low photon flux densities. Raven et al. (2000)consider the constraints on the lowest photon fluxdensities at which algal photosynthesis can occur.There are a number ofconstraints that restrict photo-synthesis and growth at low photon flux density inthe form ofenergy-consuming processes whose ratesare invariant with photon flux density, and thusconsume a large fraction of absorbed photons atlower photon flux densities. Among these processesare the redox backreactions of RCII, the leakage ofH+ through the thylakoid membrane, and the turnoverof proteins in a manner independent of the rate ofenergy supply. The first two processes limit the rateof linear electron transport and of ADP phos-phorylation respectively, while the latter consumesATP. Raven et al. (2000) emphasize that these energy-consuming processes are sequential, so that theireffects in constraining photosynthetic (and growth)rates are multiplicative. Using the data on theinfluence of these three processes on sun-adaptedorganisms (algae and higher plants) Raven et al.(2000) showed that it is difficult to explain the growthof algae at 0.5 J1ITIol photon m-2 S-I, let alone thegrowth ofthe crustose coralline red alga found at 274m where the average incident photon flux density for12 h per day not in excess of 0.02 J1ITIol photonsm-2 s-1. Further investigation is needed of how thealgae which can grow at less than 1 J1ITIol photonm? S-l cope with these energy-consuming reactionswhich use an increasing fraction ofthe energy inputas the photon flux density decreases.Turning to the shorter wavelengths (less than 400

John A. Raven and Richard J. Geider

nm), we find that UV-A (320-400 nm) can, in at leastthe short term, act in light harvesting for photo-synthesis, and also can help (as does blue light) tooffset the damage by UV-B. Corals have a host-derived fluorescent pigment that can be used toharvest UV-A under low light conditions (Salih etal., 2000). UVA can also inhibit photosynthesis inits own right. UV-B (280-320 nm) either has noeffect or, at higher flux densities, is always inhibitoryof photosynthesis and growth. There are largegenotypic differences in UV-B sensitivity amongalgae (Franklin and Forster, 1997). UV-B effectsdepend on the photon flux density of UV-A and ofphotosynthetically active radiation (Franklin andForster, 1997; Chapter 16, Franklin et al.).

B. Inorganic Carbon Supply

Inorganic carbon supply variations in the past havepresumably in part underlain the variations ininorganic carbon acquisition among the algae. Theinorganic carbon acquisition mechanism variesamong algae in terms of transport and the kineticproperties ofRubis co. Transport can be via diffusionof carbon dioxide, or pumping of CO2, bicarbonateor H+ at one or more membranes (Chapter 11,Ravenand Beardall). A carbon concentrating mechanismcan serve as ameans for concentrating CO2at the siteof Rubisco in steady-state photosynthesis to valuesabove those in the bulk medium. Regarding thekinetic properties of Rubisco, a high affinity (lowKnJ for CO2, and a high selectivity factor for CO2relative to 02' are generally correlated with a lowspecific reaction rate of the CO2-saturated carboxyl-ation reaction and vice versa (Badger ct al., 1998;Raven, 1997). The perceived requirement for ameansof concentrating CO2 at the active site of Rubisco isgreatest for organisms which normally grow at (i.e.have adapted to) low free CO2 concentrations in themedium and/or have a Rubisco with a low CO2affinity and/or a low selectivity factor for CO2over02' Furthermore, a CO2 concentrating mechanismallows the organism to fix more CO2 per unit time perunit energy, carbon and nitrogen dedicated to Rubiscoifitmaintains saturating concentrations ofCO2aroundRubisco (see Chapters 8, Beardall et al. and 11,Raven and Beardall). This is especially the case ifanorganism has a Rubisco with a high specific reactionrate (and hence generally a low CO2affinity and CO/O2 selectivity factor). A potential energeticdisadvantage of this CO2 concentrating mechanism

Chapter 17 Adaptation, Acclimation and Regulation 399

strategy comes from a consideration ofphotosynthesisand growth at low photon flux densities. The leakageofCO2 from the high concentrationmaintained aroundRubisco would constitute an energy cost that isessentially independent of the incident photon fluxdensity. This would constitute a very significantenergy loss at low light which operates in series withcharge recombination in RCII and with H+ leakthrough the thylakoid membrane (Raven et al., 2000).This problem is, apparently, dealt with adaptively bysome algae which normally grow at low photon fluxdensities and which lack CO 2 concentratingmechanisms. Some of these are red algae with veryhigh CO/02 selectivity factors for their Rubiscos,thus minimizing the energy cost associated with thephosphoglycolate synthesis which accompaniesdiffusive CO2 entry from an air-equilibrium solution(Raven et a!., 2000; Table 2). Of course, Rubiscowith a high CO/02 selectivity, low CO2-saturatedspecific reaction rate, and low Km for CO2, is notfunctioning at CO 2 saturation in today's air-equilibrium solution. To achieve a given rate ofCO2

fixation per unit biomass, an alga possessing thiskinetic variant of Rubisco operating in today'satmosphere will require higher energy, carbon andnitrogen investments in Rubisco than would the samealga operating atCO2 saturation. This is especially sofor a Rubisco with a high CO2 fixation rate per unitprotein operating at CO2 saturation.The analysis in the previous paragraph implicitly

relates to inorganic C entry from the medium into asmall cell carrying out photosynthesis with the initialcombination of CO2 into covalent linkage in anorganic C compound catalysed by Rubisco within asecond or so of inorganic C entry. In secondarilyaquatic embryophytie plants there are a wide rangeof mechanisms of inorganic C acquisition whichinvolve a preliminary inorganic C assimilation into aC4 dicarboxylie acid with a spatial (Cj-Iike) ortemporal (CAM-like) separation of the C3 + C1carboxylation and the subsequent Rubisco carboxyla-tion, with or without uptake of inorganic C fromsediment and transfer to photosynthetic structures(Raven 1984a, 1997). Such pathways are much lesscommon in, or absent from, algae (Raven, 1984a,1997).

C.pH

External pH impacts photosynthesis via the regulationof intracellular pH and the speciation of inorganic

carbon species in the medium. Species of the single-celled green algal genus, Dunaliella, can grow overthe pH range from < 1.0 to > 10.0 (Table 1; Raven,1990). As well as implications for pH regulation andthe energetics ofplasmalemma eotransport processes,including any which involve inorganic carbon, thespeciation of inorganic carbon is greatly influencedby pH (and is often a major determinant ofpH), witha temperature and salinity-dependent switch frompredominantly CO2 below pH 5.9-6.5 to predom-inantly HCO; from pH 5.9-6.5 to pH 9.2-10.5 andpredominantlycot at higher pH values. Apart fromhigh intertidal rock pools, the pH range 0.5-7.5 and8.5-11.0 in nature is essentially an inland watersphenomenon, and it is the algae of these habitats thathave adapted to very low or very high pH with theirextremes of inorganic carbon speciation. Noincontrovertible proof of direct COi- uptake asinorganic carbon source for photosynthesis has yetbeen offered (Raven, 1997).

D. Oxygen Concentration

Extremes of O2 concentration occur in nature withalgae growing in hypoxic and hyperoxie environments(Raven et a!., 1994; Chapters 8, Beardall et a!., and10, Raven and Beardall). Hypoxia is potentially aproblem for respiration in the dark phase, with littleevidence for an O2 requirement for photosynthesisper se, but rather an inhibition by O2 at low CO2

concentrations if diffusive CO2 entry to Rubiseooccurs (Raven et a!., 1994). Secondary deep chloro-phyll fluorescence maxima of Prochlorococcusmarinus populations occur in the upper regions (atdepths of 80-140 m) of the oxygen minimum zones«10 pM O2) ofthe Arabian Sea and EasternTropicalNorth Pacific Ocean (Goericke et a!' 2000). Here, theabilities to use low light «1 to 20 ,umol photonsm-2 S-I), and withstand hypoxic conditions allowsP marinus to exploit a novel niche in the open ocean.Hyperoxia up to several times the present air-

equilibrium level can occur in high intertidal rockpools, in many bodies of freshwater, and in someorganisms with CO2 concentrating mechanisms evenwith external normoxia. Tolerance ofhyperoxia maybe improved by higher levels ofenzymes that removeactive oxygen species (Raven et a!., 1994,1998).However, some hyperoxia-tolerant algae do not havevery high levels of enzymes which remove activeoxygen species (Raven et a!., 1994, 1998). Most ofthe enzyme-catalyzed O2 uptake reactions which

400

generate active oxygen species have a relatively highaffinity for 0z' i.e. are at or near saturation at air-equilibrium concentrations of 0z in solution.However, some active oxygen species may begenerated by non enzyme-catalyzed reactions of O,with reduced redox intermediates, and the rates ofsuch reactions are directly proportional to theconcentration ofO, (provided that the concentrationofthe reduced redox intermediate does not vary withO, concentration). Such reactions include thereduction ofO, to°2' by PQ'- (in plastids) or UQ'-(in mitochondria). Although this reaction is notthermodynamically favored, since the redox potentialofthe 0/02'- couple is more negative than that ofthePQ'-/PQ or UQ'-/UQ couples, it does occur to someextent (Raven et al., 1998).

E. Temperature

Adaptation to different temperatures for growthinvolves changes in the degree ofthylakoidmembranelipid saturation, the kinetics and quantity ofenzymessuch as Rubisco, and the ratio of light-harvestingpigments to downstream catalysts, in all casescompared to phylogenetic ally closely relatedorganisms adapted to a different temperature regime.Adaptation to lower temperatures involves less-saturated thylakoid (and other membrane) lipids,and a lower ratio ofantenna pigments to downstreamcatalysts (Geider, 1987; Raven and Geider, 1988).The very high sensitivity ofzooxanthellate corals tosmall rises in summer temperatures, manifested incoral bleaching, is described in Chapter 19 (Yellow-lees and Warner).

F. Pressure

The extent to which the pressure component ofwaterpotential impacts on photosynthesis is limited by themaximum depth to which sufficient photosyn-thetically active radiation penetrates, with the limitfor benthic algae of274 m corresponding to a pressureof2.74 MPa in excess of atmospheric (0.1 MPa). Ofcourse, even if photosynthesis in excess ofrespirationover 24 h cannot occur at depths below 274 rn,planktonic algae can be circulated down to greaterdepths or sedimented to, and then resuspended from,greater depths, and retain their photosyntheticcapacity. It is not clear ifthere are specific adaptationsof algae to pressure tolerance. That phytoplanktoncan tolerate a pressure of 10 MPa in excess of

John A. Raven and Richard J. Geider

atmospheric was shown by Platt et aI. (1983) whofound that the light-saturated photosynthesis rates ofphytoplankton sampled from 10 and 1000 m weresimilar when incubated on deck. The light-limitedinitial slope and susceptibility to photoinhibitionwere higher in the sample collection from 1000 m, asexpected if this population had acclimated to lowlight during transit to 1000 m. There are certainlyadaptations to external osmolarity (the osmoticcomponent ofwater potential) in the form of activewater efflux from (functionally) wall-less cellsgrowing at low osmolarities and the production ofcompatible solutes in the cells oforganisms growingat higher external osmolarities.

VI. Acclimation of Algal Photosynthesis

Variations of chlorophyll a-specific photosynthesisrates and chlorophyll a-specific light absorptioncoefficients are evident in natural populations ofmarine phytoplankton (Kyewalyanga et aI., 1998).These variations can arise from replacement of onepopulation or assemblage ofphytoplankton by anotherpresumably better-adapted assemblage (successionor competition), or by physiological acclimationwithin a population or assemblage. Much of thevariability in biomass-specific photosynthesis onseasonal time scales appears to be related to changesin species composition (Cote and Platt, 1983).However, photoacclimation is evident in verticaldistributions of cell pigment content (Campbell etal., 1994), chlorophyll a-specific light-saturated andlight-limited photosynthesis rates (Platt et aI., 1982),and chlorophyll a-specific light absorption coef-ficients (Mitchell and Kiefer, 1988). Whether thesevertical gradients of physiological responses arestrictly due to acclimation, or are due to a combinationof acclimation and adaptation (or competitiveexclusion) is an area that deserves further research.Photoacclimation involves co-ordinated changes

in the composition and functioning of the photo-synthetic apparatus in response to variations ofphotonflux density. Several strategies of photoacclimationin phytoplankton have been elucidated, based onchanges in the photosynthetic unit size, photosyn-thetic unit number per cell, and Calvin-Benson cycleactivities per cell (Richardson et aI., 1983; MacIntyreet al., 2002). Although commonly described in termsof responses to the incident irradiance, themechanisms underlying photoacclimation is likely

Chapter 17 Adaptation, Acclimation and Regulation 401

to involve the cell's perception of the rate of lightabsorption (Kana ct al., 1997) rather than theirradiance per se. For example, the chloro-phyll a:carbon ratio can be described as a function ofthe rate of light absorption in Skeletonema costa tumeven though chlorophyll a:carbon varies by over afactor of two as a consequence of variations inspectral quality at a given photon flux density (Nielsenand Sakshaug, 1993).Phytoplankton absorb a variableproportion of the photons incident on their surface(Bricaud and Morel, 1986). In addition, because theabsorption spectrum of phytoplankton is not flat(Bricaud andMorel, 1986), the rate oflight absorptiondepends not only on the irradiance, but also onspectral quality of the underwater light field and theabsorption spectrum of the phytoplankton.Photoacclimation involves changes in the com-

position and cellular abundance of light-harvestingpigment-protein complexes, in the cellular abun-dances and ratios ofPS I:PS II reaction centers andofother catalysts within the electron transport chainand changes in the abundance of Calvin-Bensoncycle enzymes, most notably Rubisco (Sukenik etal., 1987).Photoacclimation can also result in changesofphotoprotective pigments (MacIntyre et al., 2002)and antioxidant defenses. Photoacclimation responsesdepend in part on whether the photon flux density ofphotosynthetically active radiation is light-limitingor light-saturating for growth. These two regions canbe delimited by specifying the saturation irradiance(Ik) defined as the ratio of the light-saturated growthrate to the initial slope ofthe growth versus irradiancecurve (Fig. 3A). Relative changes of cell pigmentcontent, photosynthetic unit size and photosynthesis-irradiance response characteristics tend to scale withI/Ik (Fig. 3). Thus, knowledge of I/Ik providesconsiderable insight into the photoacclimatoryresponse of nutrient-replete algae (MacIntyre et al.,2002). Marked increases ofphotosynthetic unit size(as defined by the ratio oflight-harvesting pigmentsofPS II reaction centers) tend to accompany growthat irradiances less than Ik (Fig. 3C, D). The number ofphotosynthetic units per cell (or per unit cell biomass)also tends to be greater in low-light growth conditions.The photoacclimation of many photosynthetic

characteristics is typically a continuous function ofphotonl1ux density (Fig. 3). Therefore, it is incorrectto speak of high-light versus low-light-acclimatedcells. Rather, cells acclimate along a continuum thatcan be defined by I/Ik (MacIntyre et al., 2002). Aswith adaptation to low photon flux densities,

acclimation to different photon flux densities forgrowth often involves a larger photosynthetic unitsize, with similar numbers ofPS I and PS II reactioncenters per cell (for unicells) or per unit thallus area(for macrophytes). In some cases the photosyntheticunit size is invariant with photon flux density (forunicells) or per unit thallus area (for macrophytes).In some algae the PS l:PS II ratio increases at lowphoton flux density (Raven et a1., 1999).Whether acclimation to lowerphoton flux densities

involves larger photosynthetic unit sizes or morephotosynthetic units, it always involves an increasein cellular pigment content leading to a higher opticalthickness, and hence a greater package effect. Thishas implications for the time taken, in a given radiationenvironment, to absorb the photons needed to supplythe energy required to synthesize the photosyntheticpigment-protein complexes (Raven, 1984a). Ofcourse, the range of absorptances, and hence ofpackage effects and the time taken to recoup con-struction costs, which occurs via acclimation in agiven genotype is much less than the range found byadaptation in algae as a whole.Recent evidence suggests that photoacclimation

occurs in response to a signal transduction mechanismthat involves the redox state of one or more com-ponents of the photosynthetic apparatus (Eseoubaset al., 1995;Maxwell et a1., 1995). Most attention hasbeen focused on the ratio of reduced to oxidizedplastoquinone (PQH/PQ) (Allen, 1993; Escoubas etal., 1995; Pfannschmidt et a1., 1999).The ratio PQH/PQ appears to be an attractive signal because itprovides a direct measure ofbalances or imbalancesin the functioning of the photosynthetic electrontransfer chain (Chapter 13, Larkum).Changes in expression of light-harvesting

complexes, or light-harvesting complexes plusthylakoid redox components, or of PS II relative toPS I, can be related to the PQH/PQ ratio (Allen,1993; Pfansschmidt et al., 1999). A high PQH/PQratio indicates a high excitation energy input to PS IIrelative to the capacity for CO2 fixation, via PS I andthe cytochrome bJcomplex. A high PQH/PQ ratiosignals to the gene transcription system that thelight-harvesting apparatus needs to be downregulatedsuch that the excitation energy input to PS II isrestricted. This ismost readily achieved by decreasingthe size of the photosynthetic unit for PS II ratherthan via fewer PS II with a similar, or smaller,complement of PS 1. Conversely, a low PQH/PQindicates a low excitation energy transfer to PS II

402 John A. Raven and Richard J. Geider

2.2r--r

IQ) 1.0

1---GiT-- -----EJ-

I+-' @ A v Bco 1.80::: U 8 I0.8

I..c I - D

1: ..c 1.4 I0 0.6 ~ ~

o 8'.... Q) D;(9

04~> 1.0 -'-G---------

Q):;:;co v

> Q) 0.6D

:;:; d7co 0:::Q) I

0

0:::0.2 j

0.2I0.0 --.-----r--"

0 1 2 3 4 5 6 7 0 1 2 3 4 5 6 71.6 ----------- 1.6

0

I1.4 C 0 1.4 . 0 D(f) 0

II"-

D I0.. 0..1.2 0 1.2 g I<tl v I <tl

s: 0 ..c coU 1.0 ~v__________ U 1.0 I--u- -- --.------Q) vI ~

Q) v> ~ > I ~ ge>+-' 0.8 :;:; 0.8co I co IQ) Q)

0::: 0.6 I 0 0::: 0.6 I0

0.4 0.40 1 2 3 4 5 6 7 0 2 3 4 5 6 7

31.4

I E I FI

cIs: 1.2 0

0

t)I 0

v vvI(f)

Q) vo+." 0..001

0

°.?: 1.0 - -'----- "------ --- 2 v 0+-' 0co D vI u 0 0

IQ)t-,v D 0.. v

0::: 0.8 I vD I0I I 0 I D 0

0.6

I- I Ii - ---i-----------r---· i---

0 1 2 3 4 5 6 7 0 2 3 4 5 6 7

I/Ik I/IkFig 3, Photoacclimation ofthc marine diatom Thalassiosira weissfloggi (inverted triangles), the haptophyte Isochrysis galbana (circles)and the dinoflagellate Prorocenlrum micans (squares) to growth at irradiances of 30 to 600 ,umol photons m-2 S-l, Irradiance has beenexpressed relative to Ik , (A) Relative growth rate versus IIIk. (B) Relative chlorophyll a:carbon versus I!Ik. (C) Relative Photosystem IIunit size (chlorophyll a per 02 evolved per saturating flash) versus IIIk, (D) Relative Photosystem I unit size (chlorophyll a per P700 versusIIIk, (E) Relative chlorophyll a-specific initial slope of the photosynthesis-irradiancc response curve (cfhl) versus IIIk, (F) Absolute PSII:PS I ratio versus IIIk . Absolute values of these variable at an irradiance of 150 ,l/lnolphotons m-

2 s-l are given in Table 3, Based on datafrom Falkowski et al. (1985) and Dubinsky et al. (1986), Although there have been a number of other studies where photosyntheticcharacteristics have been examined in cells acclimated to a range ofgrowth irradiances, very few have all the data required to plat in themanner illustrated in this figure,

Chapter 17 Adaptation, Acclimation and Regulation 403

Table 3. Interspecific variability of photosynthetic characteristics of selected marine phytoplankton. Observations from Falkowski et aI.(1985) and Dubinsky et aI. (1986)

Species Growth Ill k 2 Growth Chla:C 4 aChl5 aChl 6 PSUo/ P700 8 PS II1PS [9Irradiance ' Rate 3

Thalassiosira 150 0.75 1.15 0.035 4.2 0.37 2,340 1,350 1.7weissfiogii

lsochrysis 150 1.5 1.1 0.014 11 1.2 1,554 835 2.1galbana

Prorocentrum 150 .75 0.11 0.0046 12 0.78 2,350 855 I.5micans

Units are as follows: I Jl!TIo[ m- 2 s"; 2 dimensionless; 3 d"; 4 gig; Slight absorption coefficient, m? g! ChI a; 6 chlorophyll a-specific initialslope; m- (g I chla) mol 02 (moll photons); 7 mol chlorophyll a (mol 02 in a saturating flash):"; Hmol chlorophyll a (mol P700t 1; 9dimensionless

relative to the capacity for downstream processes,and signals the increased expression of light-harvesting antennae pigments, with or without anincrease in the number of PS II units per cell or perunit thallus area.It is not certain that PQH/PQ ratio is the sole

regulation of the differential expression ofgenes forredox and related reactions of photosynthesis inresponse to variations in the incident photon fluxdensity. It does, however, seem plausible that thePQH/PQ ratio should be the determinant of differ-ential expression of genes associated with 'comple-mentary chromatic acclimation' in those algae,especially members of the Cyanobacteria and theRhodophyta, which have very different spectralabsorptances of the pigments supplying energy prin-cipally to PS II (phycobilins with aminor componentof chlorophyll a) relative to those supplying energyprincipally to PS I (predominantly chlorophyll a).Organisms acclimated to a predominantly green(phycobilin-absorbed) photon input for growth wouldhave a lowphycobilin to chlorophyll a ratio. Switchingthe photon input to red or blue wavelengths (i.e.mainly absorbed by chlorophyll a) decreasesenergization of PS II, lowers the PQH/PQ ratio,leading to increased expression ofphycobilins. Thisbrings absorption by phycobilins (supplying PS 11)and chlorophyll a (mainly supplying PS I) closer tothe 1:1 ratio required by linear electron transport.Allen (1993) has suggested that the retention of

some ofthe original endosymbiont genes by plastids(and mitochondria), rather than their transfer to thenucleus (or their complete loss), is related to theregulation ofexpression oforganelle-encoded genesby organellar redox state as an indication of

environmental conditions. Allen and Raven (1996)point out that the potential for mutation oforganellegenomes as a result ofactive oxygen species producedin the organelle redox reactions might favor genetransfer to the nuclear genome. As the number ofphotosynthetic (or respiratory) genes retained in theorganelle decreases, the marginal cost of theremaining bioenergetic genes is increased since thegenes for replication, transcription and translation inthe organelle must be retained for an ever-smallernumber of bioenergetically active genes. While thesuite of genes retained in plastids shows significantvariation among higher taxa of algae, there is a coreof genes in all of the plastids that have beeninvestigatedwhich code for one or more componentsof PS 11, PS 1, the cytochrome b.f complex andRubisco. The extent to which the presence of thesegenes in the plastid genome improves (e.g. speedsup, ormakes more precise and accurate) the regulationof their expression in response to environmentalcues needs further investigation, as does thesignificance ofthe phylogenetic variation in the suiteof genes present in plastids. However, it is certainlypossible that the variation in genes retained by theplastid genome can influence the rate or extent ofacclimation of the photosynthetic apparatus.The aeclimatory processes described above have

been modeled by Geider, McIntyre and Kana (1996)for phytoplankton cells. The key feature ofthe Geideret al. (1996) model is that the signal for acclimationof pigment content is assumed to be directly relatedto the quantum efficiency of photosynthesis. It is ofinterest that the observed changes in content ofphotosynthetic catalysts which Geider et al. (1996)model do not require increased rates of degradation

404

of catalysts whose content per cell decreases duringacclimation in a growing cell population. This meansthat dilution during growth can account for theobserved changes, and the enhancement (or initiation)ofdegradative reactions is not needed to explain thedynamics of these components whose content percell is decreased during acclimation. It should benoted, however, that there are only two data sets thatprovide the necessary information for the Geider etal. (1996) formulation to be rigorously tested. Bothof these data sets are for diatoms that can grow overa wide range of photon flux densities. Otherorganisms, in particular the Cyanobacteria whereactive degradation of phycobilisomes has beendocumented in response to nutrient limitation, mayemploy different mechanisms.Whether a species employs dilution or degradation

(turnover) to decrease pigment content followingtransfer to high irradiance may depend on the extentto which excitation energy transfer from the pigmentbed to the reaction centers is subject to regulation.Diatoms can down-regulate excitation energy transferto PS II when exposed to saturating photon fluxdensities. This is an important safety valve whichallows the diatoms to retain pigments without placingundue excitation pressure on PS II. This, in turn,minimizes the potential for photoinhibition andphotooxidative stress. In contrast, Cyanobacteria lacka xanthophyll cycle, and (with the exception notedabove) appear to be unable to effectively quenchexcitation energy in the phycobilisomes. In addition,diatoms continue to synthesize diadinoxanthinfollowing transfer to high light, whereas furtherprocessing of diadinoxanthin to fucoxanthin isinhibited. This allows diatoms to synthesize theprecursor to a light-harvesting xanthophyll duringexposure to bright light, and subsequently to rapidlytransform the precursor (diadinoxanthin) into thelight-harvesting fucoxanthin after return to low light.Thismaybe particularly advantageous in a chronicallylow-light environment that is punctuated by briefexposure to bright light. Such an environment isexperienced by cells cycling vertically in an opticallydeep mixed layer characteristic of the spring bloomconditions in temperate zones. If the diadinoxanthinalso participates in the dd-dt cycle-related non-photochemical quenching, then there may be anadded bonus of increased non-photochemicalquenching during the bright-light exposure. If themechanism of photoacclimation to bright light inCyanobacteria involves active pigment degradation,

John A. Raven and Richard J. Geider

than Cyanobacteria would be at a disadvantage inwell mixed water columns.Another acclimatory mechanism that is driven by

variations in photon supply is the variation of theratio ofxanthophyll cycle carotenoids (violaxanthin!antheraxanthin/zeaxanthin and/or diatoxanthin/diadinoxanthin) to PS II reaction centers which oper-ates in all higher algal taxa investigated except forthe Cyanobacteria and most Rhodophyta (seeFalkowski and Raven, 1997; Ursi et al., 2003). Thismechanism operates by the altering the quantity ofexcitation energy reaching PS II relative to thecapacity for downstream processing of electrons,Here it is possible that a high PQH/PQ ratio, signalinga potential excess ofexcitation energy reaching PS IIto photochemical sinks for the energy, leads to thesynthesis ofmore xanthophyll cycle carotenoids perPS II reaction center. However, the phenomenon ofacclimation of xanthophyll cycle components hasonly been documented in a few algal species and itsregulation is poorly documented (Falkowski andRaven, 1997).Acclimation of the photosynthetic apparatus to

variations in the supply of certain elements can, invarious taxa, involve changes in the light harvestingantenna complexes of certain freshwater Cyano-bacteria and in marine Cyanobacteria with the lowFe effect on isiA (Bibby et al., 2001a; Boekema et al.,200 I). It can also involve the water-soluble redoxagents involved in electron transfer from thecytochrome bdto p~oo and from the reducing end ofPS I to the ferredoxin-NADp t oxidoreductase (Ravenet al., 1999). Growth of Cyanobacteria under S-deficient conditions can lead to the replacement ofthe usual phycobilins with phycobilins whose proteinscontain less cysteine, i.e. less S (Maze Iand Marliere,1989).The soluble redox protein in the thylakoid lumen

which transfers electrons from the cytochrome bdcomplex with P~oo is either the Fe-containing cyto-chrome c6 (Rhodophyta, Heterokontophyta, Hapto-phyta(?), Euglenophyta), the Cu-containing plasto-cyanin (some Chlorophyta) or, in the cases ofinterestin terms of acclimation, either cytochrome c, orplastocyanin (Cyanobacteria, some Chlorophyta).The expression of cytochrome c6 or plastocyanin inthe organisms which produce either is regulated bythe availability of Fe relative to Cu in the growthmedium. A limited supply of Fe relative to Cu leadsto the expression of cytochrome c6 rather thanplastocyanin, while a restricted supply ofCu relative

Chapter 17 Adaptation, Acclimation and Regulation 405

to Fe leads to the expression of plastoeyanin ratherthan cytochrome c6•The fraction ofthe total catalyticFe in an algal cell which occurs in cytochrome ismuch smaller than the fraction of total catalytic Cuwhich occurs in plastoeyanin. Thus, the expressionofcytochrome c6 rather than plastocyanin results in agreater proportional saving in catalytic Cu than thesaving in catalytic Fe resulting from the expressionof pIastocyan in rather than cytochrome c6 (Raven etaI., 1999).The final catalyst substitution concerns the

replacement of the normal agent, the Fe-containingferredoxin, with the metal-free flavodoxin, as thecatalyst of electron transfer on the cytosol (Cyano-bacteria) or stroma (eukaryotes) from the reducingendofPS I to the ferredoxin-NADP' oxidoreductase,and thence to NADP' (see Raven et al., 1999). Inmany, but by no means all, algae, Fe deficiency in thegrowth medium leads to the expression offlavodoxinrather than ferredoxin. Deficiency in this contextdoes not necessarily mean that the availability ofironis so low as to restrict growth rate under otherwiseoptimal conditions (McKay et al., 1999; Davey andGeider, 200 I). However, the detection of flavodoxinhas been used as a biological marker of incipient andactual Fe deficiency in natural assemblages ofmarinephytoplankton (La Roche et al., 1996; Erdner andAnderson, 1999; Erdner et aI., 1999). It is of interestthat a red alga (Chondrus crispusy appears toconstitutively express flavodoxin, with no capacityto produce ferredoxin; this needs to be followed upby molecular genetic approaches.Having considered in at least semi-quantitative

terms the benefits of the acclimatory substitutionsamong proteinaceous catalysts with different contentsof S, Fe and Cu, it is appropriate to ask if there arecosts of substituting a catalyst which has less, ornone, or some, ofthat clement. For the low-cysteinephycobilins, economizing in S,we do not know if theS-economical variant has a similar capacity to absorbphotons and transfer excitation energy to that of themore S-demanding variant. In the case ofcytochromec6 and plastocyanin it appears that these two catalystshave equal catalytic potential, regardless ofwhetherthey are tested in (where appropriate) homologous orheterologous thylakoid systems. For the ferredoxin!flavodoxin pair it appears that the Fe-containingferredoxin has a greater catalytic potential (molelectron transferred per mol catalyst per second) forelectron transfer from PS I to ferredoxin-NaDf"oxidoreductase than does the metal-free flavodoxin.

Acclimation to variations in 02 levels can involvechanges in scavengers and quenchers ofaetive oxygenspecies such as singlet-oxygen and the hydroxylradical, and enzymes which remove the active oxygenspecies superoxide and hydrogen peroxide (Raven etal., 1994). However, variations in 02 concentrationdo not alwaysyield acclimatory changes in scavengerssuch as ascorbate or in the enzymes superoxidedismutase and ascorbate peroxidase (Raven et al.,1998).Variations in inorganic C supply involves

acclimation ofthe inorganic C acquisition mechanismexcept for those organisms which reply only ondiffusive CO2 entry and cannot express aCO2 concen-trating mechanism (Chapter 11,Raven and Beardall).The possibility that the morphology ofbcnthic macro-algae using diffusive CO2 entry may change as afunction of inorganic C concentration (freshwater)or water flowregime (freshwater or the sea) in relationto diffusive CO2 supply does not seem to have beeninvestigated. Of course, algae with carbon concen-trating mechanisms might also show morphologicalchanges in response to variations in the diffusivesupply of inorganic carbon to the thallus surface inaddition to the cell-level acclimation discussed below.The observed changes in inorganic carbon

acquisition kinetics when algae which can express aCO2 concentratingmechanism andwhich are growingwith an unrestricted inorganic C supply are switchedto a restricted inorganic C supply is an increase in theaffinity for inorganic carbon. There is a wide range ofmechanisms of CO2 accumulation underlying theacclimation process in different organisms, and thereis sometimes more than one mechanism of CO2accumulation involved in a single genotype. Qual-itative or quantitative changes in the expression ofcatalytic mechanisms associated with CO2 accumu-lation inelude periplasmic and intracellular (mito-chondrial, stroma/cytosol, thylakoid) carbonicanhydrases, and of transporters at the plasmalemmaand/or plastid envelope, involving ATP-driven CO2orHC0:Jpumps, HC0:J/CI-orHCO/OH- antiporters,or redox-associated inorganic C pumps (e.g. NADHdehydrogenase in Cyanobacteria which is involvedin uptake of inorganic C from the medium anddelivery ofHC0:J to the cytosol) (Poole and Raven,1997; Raven, 1997; Axelsson et al., 1999; Ornata etaI., 1999).These data show widespread occurrence of

acclimation of these inorganic carbon acquisitionmechanisms to variations in inorganic carbon supply

406

across a wide taxonomic range and a diversity ofmechanisms. It is not clear what signal transductionpathway converts the environmental signal to thechanged algal performance in any system, so that itis premature to ask if similar signaling systems areinvolved in the diversity of CO2 accumulationmechanisms in the range of organisms.It is also important to ask what the ecological

relevance of these acclimatory responses. In highintertidal rock pools, or freshwaters with relativelylow inorganic C:N or inorganic C:P ratios, there aresignificant changes in inorganic C acquisitionresponses by algal genotype as a function ofdifferences in concentration and speciation ofinorganic C. The range of variation of marinephytoplankton C, Nand P contents is reviewed byGeider and La Roche (2002). Even for organismsliving in habitats with a more constant inorganic Csupply there are acclimatory responses of the CO2concentrating mechanism. It is possible that theseacclimatory responses relate to variation in otherresource-supply, and other environmental, variableswhich interact with CO2 concentrating mechanisms.It is known that CO2 concentrating mechanisms inCyanobacteria (Beardall, 1991) and eukaryoticmacroalgae (Kiibler and Raven, 1995) show inverseeffects of reduced inorganic C supply and lowerincident photon flux densities. Interactions ofinorganic N, Fe and Zn supply with CO2concentratingmechanisms are predicted; interactions among thesenutrients and have been found experimentally, butnot always as predicted (Raven, 1991, 1997; Fal-kowski and Raven, 1997; Erica Young, personalcommunication).Temperature acclimation by algae is considered

byAIming et al. (2001) and Raven and Geider (1988).

VII. Regulation of Algal Photosynthesis

Regulation refers to the control of enzyme activityand energy dissipation pathways that occursindependently of net macromolecular synthesis ordegradation. Regulation will be considered in termsof the (apparently) important physiological andecophysiological functions that they perform and thecatalysts which are regulated rather than categorizingthem according to the means by which regulation isachieved, although the three processes we considerhave different means of modifying the catalysts.The first regulated process that we consider is the

John A. Raven and Richard J. Geider

activity ofRubisco, i.e. the enzyme activity per unitof enzyme protein. MacIntyre et al. (2000) point outthat short-term (tens of seconds-minutes) activationand deactivation of Rubisco can account for short-term variations in maximum photosynthetic rates in(for example) rapid changes in photon flux densityduring mixing in the surface mixed layer. Changes inthe activation state of Rubisco may also underlieadjustment to steady-state photon flux densityvariations over time too short to permit acclimation(change in Rubisco protein content). Activity changesof Rubisco in algae appears to be dependent oncarbamylation and decarbamylation and, perhaps,the level of tight-binding inhibitors such ascarboxyanobinitol-l-phosphate. The role ofRubiscoactivase in regulating Rubisco activity in algae andCyanobacteria is not clear; this enzyme is present inChlamydomonas and, apparently some filamentousCyanobacteria, but not the unicellular cyano-bacterium Synechocystis PCC 6803 (Kaneko et al.,1996; Li, Zianni and Tabita, 1999). Since the rate ofactivation ismuch faster than the rate ofdeactivation,Rubisco may remain in an active state during short-term fluctuations in photon flux density (e.g. duringrapid vertical movement in high-attenuation habitats,such as an estuary; MacIntyre et aI., 2000).A second regulated process which occurs over a

time course ofminutes is the state transition phenom-enon. This changes the relative absorption by thePS I and PS II antennae by reversible dissociation ofsome pigment-protein complex from PS II (with orwithout reversible association with PS I), and (as wehave already seen) state transitions occur in greenalgae, red algae and Cyanobacteria (Table 1)(Chapter13,Larkum). Phosphorylation and dephosphorylationappear to underlie these responses. High irradiation,and darkness favor state I (preferential excitation ofPS I), while excess excitation ofPS I (e.g. by red-farred light) favors state II (preferential excitation ofPS II). State transitions alter the photosyntheticeffectiveness oforganisms by excitation energy arrivalat the limiting photoreaction centers (PS II or PS I),and thus altering efficiency ofphotosynthesis at lowphoton flux densities and the extent of diversion ofexcitation energy from PS II at high incident photonflux densities.A third regulated process is the xanthophyll cycle

in all ofthe algae investigated except Cyanobacteriaand most of the red algae (Chapter 13, Larkum; Ursiet aI.,2003), and the phycoerythrobilin-phycourobilininterconversion in the cyanobacterium Tricho-

Chapter 17 Adaptation, Acclimation and Regulation 407

_ State transitions

VIII. Rates of Regulation and Acclimation

..--.~ PSll photodamage and repair

_ Rubisco activation/deactivation

Fig. 4. First order time constants for acclimation of algalphotosynthesis to step changes in photon flux density. figureprovided by Hugh Maclntyre (Horn Point EnvironmentalLaboratory). Updated from Macintyre et al. (2000).

and is reversible on short time scales (seconds to tensof minutes), acclimation involves the net synthesisand breakdown of macromolecules. As such, theachievable rate ofacclimation to changing conditionsis limited by the mechanistically achievable rates ofmacromolecule synthesis and/or degradation andwhat is selectively appropriate, granted the timecourse of environmental fluctuations.Light is clearly the most rapidly varying environ-

ment factor, and one whose tracking by acclimationis likely to be costly in energetic (and C andN) terms.As such, rapid variations oflight environment inducea number of regulatory responses. Over the longerterm, phytoplankton appear to acclimate to theequivalent in terms of a steady photon flux densitywhich is rather higher than the arithmetic mean ofthe varying photon flux densities which occur duringthe photoperiod (Gilstad et a!., 1993; Kromkampand Limbeek, 1993; Flameling and Kromkamp,1997). The algae thus appear to be acclimated tovariations in photon flux density in a manner whichprotects against photoinhibition in high photon fluxdensities rather than maximizing performance at thelow photon flux density extreme of the variation.This procedure may limit restrictions on thephotosynthesis during low photon flux densityepisodes due to photo-damage incurred in high photonflux density episodes; this damage (or photo-protective procedures) restricts photosynthesis at lowphoton flux densities to a relatively greater extentthan at high photon flux densities.Inorganic carbon concentrations can change such

that free CO2 concentrations can vary by an order ofmagnitude in an hour, and the resource cost ofacclimation is relatively high if significant changesin Rubisco arc involved. However, acclimation oftransporters, carbonic anhydrases and photores-piratory cycle enzymes (or their surrogates inglycolate metabolism) to CO 2 availability have lowerresource costs (Raven, 1991).The costs ofacclimationto S deficiency by replacingmajorprotein components(phycobilins of Cyanobacteria) with low-S homo-logs (Mazel and Marliere, 1999) can also be high,even ifmany of the amino acids used are scavengedfrom the high-S phyeobilins which are degraded.Addressing N, P and Fe deficiency by increasingexpression oftransporters has a relatively low cost inenergy, C and N, as has switching from ferredoxin toflavodoxin and cytochrome c6 to plastocyanin as ameans of economizing on Fe in catalysts. There arealso changes in quantities ofcatalysts which contain

mill secI I II Time100 10-1 10-2 (min)

_ Xanthophyll cycle

hourII I102 10'

Many regulatory reactions occur so rapidly as toallow photosynthesis to track instantaneously thenaturally occurring changes of environmentalconditions (i.e. they have time constants of secondsor less) (Fig. 4). These include, for example the light-dark activation-deactivation of fructose-l,6-bisphosphate (and sedoheptulose-l,7 bisphosphate)-l-phosphatase; this takes place over seconds. Anotherexample is activation-deactivation of the CFO-CFl'ATP synthetase. Other regulatory mechanisms, suchas the three outlined in the previous section, occurwith time constants of minutes, and as such mayconstrain rates ofphotosynthesis or photoprotectionin rapidly changing light environments (MacIntyreet aI., 2000).Unlike regulation, which typically occurs rapidly

-J1m_ Chlaquota

• • pChlm

desmium (see above). This process occurs over time-scales ofminutes, and involves covalent modificationto the chromophores which varies the capacity toquench excitation energy. The high-quenching formsof the pigments restrict excitation energy transfer toPS II, thus down-regulating PS II activity but alsothereby limiting photodamage to PS IT. Thisproduction of the pigment from which quencherexcitation energy occurs when organisms arc exposedto high photon flux densities, and involves activity ofde-epoxidase enzymes in the xanthophyll cycle andphycoerythrobilin to phycourobilin conversion inTrichodesmium. De-epoxidation predominates underlow irradiances.

weekdavI I"I

104 10J

408

Fe and for which no non Fe-containing analoguesoccur. The concentrations ofnutrients such as S,N, Pand Fe usually vary rather slowly in the algalenvironment. However, rapid enrichment of themedium for phytoplankton results from mixing ofdeeper nutrient-richwater into the upper mixed layer/epilimnion and rapid deprivation and reinstatementofnutrients to intertidal marine algae occurs with theebb and flow of tides.What we know of time courses of acclimation to

changes in resource availability is generally derivedfrom the imposition of step changes in resourceavailability. For uptake and assimilation of chemicalresources and replacement ofcatalysts with analogueswhich use less (or more) of a resource the half-timeof acclimation at 20-25 °C is, even for the mostrapidly growing algae, an hour or more. The timetaken cannot be directly related to the quantity ofmaterial to be synthesized. For decreases in catalyticactivity dilution during growth may occur with nofurther net synthesis until the new steady level hasbeen achieved (Geider et al., 1996, 1998). Forexample, cell chlorophyll a content declines due toaccelerated cell division without net breakdownfollowing transfer from low to high light (Cullen andLewis 1988; Arming et aI, 2000; MacIntyre et al.,2002). The change off1avodoxin abundance followingresupply of iron to Fe-limited cells appears to occurby dilution rather than by active breakdown (Daveyand Geider, 2001). In some cases a turnover ofcatalysts can speed net decay if synthesis is decreasedor abolished but breakdown is not (see above). Thetime taken for responses ofcatalysts to Fe deficiencyis relatively slow,perhaps because large-scale changesin major photosynthetic catalysts is involved. Theselengthy time courses of acclimation resemble thoseto variations in photon flux density where half-timesof response of hours to step changes in photon fluxdensity are common, even for rapidly-growingmicroalgae. The long half-time for acclimation tostep changes in photon flux density contrasts withvery rapid changes in photon flux density in thenatural environment, e.g. cloud changes, wavefrequency, and circulation in the upper mixed layer/epilimnion, with frequencies of seconds to tens ofminutes (Gilstad et al., 1993; Kromkamp andLimbeek, 1993; Flameling and Kromkamp, 1997;Raven and Kubler, 2002.An important development since the late 1970s

has been the formulation ofmodels that quantify the

John A. Raven and Richard J. Geider

changes in photosynthesis and growth of algae as afunction of variations in light, nutrients andtemperature. These models can be used to relate cell-level phenomena to algal ecology (MacIntyre et al.,2000). Most of the earlier models (Shuter, 1979;Laws and Bannister, 1980; Kiefer and Mitchell,1983) were developed for conditions of balancedgrowth, and typically invoke, optimally, criteria basedon maximizing the efficiency ofresource use in theirformulations. However, some recent models (Kanaet al., 1997; Geider et al., 1998) are dynamic in thesense that they are formulated for unbalanced growthin variable environments. They have been based onsimple regulatory rules that do not necessarilymaximize resource use (Geider et al., 1996, 1998;Kana et al., 1997) and/or simplified treatments ofbiochemical pathways (Flynn et al., 1997; Flynn andHipkin, 1999). Validation of earlier models waslimited to comparisons with balanced growthconditions in chemostat cultures. The recent modelshave been applied to batch cultures (Flynn et al.,1997; Geider et al., 1998) as well as to step-changesof photon flux density (Geider et al., 1998; Flynn etal., 200 I). Suchmodels must tread a fine path betweenundue simplification which may neglect importantbiochemical and biophysical phenomena and morecomplexity than is useable in analyzing laboratoryand, especially, field data (Geider et al., 1998). Thefurther development of such models is limited bygaps in our understanding of the mechanisms ofregulation and acclimation as well as by theavailability ofsuitable data sets for model validation.

IX. Conclusions

Our understanding of adaptation, acclimation andregulation in algal photosynthesis has advancessignificantly over the last decade. The advance ingenome analysis of Cyanobacteria is greatly aidingour understanding of photosynthetic adaptationamong Cyanobacteria, especially with respect tolight use and inorganic carbon use. Genomics arealso helping our understanding of acclimation inCyanobacteria by indicating the range of geneticoptions for light harvesting and inorganic carbonacquisition and the conditions in which these optionsare exercised. Modeling is also increasinglysignificant in synthesizing data and in predicting theoutcomes of environmental variations.

Chapter 17 Adaptation, Acclimation and Regulation 409

Acknowledgments

Work on adaptation and acclimation ofalgal growthand photosynthesis in the JAR's laboratory is fundedby The Natural Environment Research Council UKand has been funded by the Scottish ExecutiveEnvironment and Rural Affairs Department and inRJG's laboratory by The Natural EnvironmentResearch Council UK. We thank Dave Suggett forproviding Fig. 1 and Hugh MacIntyre for providingFig. 4.We also thank Marcel Vcldhuis for providingunpublished data that was used in construction ofFig. 2.

References

Allen JF (1993) Redox control of gene expression and thefunction of chloroplast genomes-i-an hypothesis. PhotosynthRes 36: 95-102

Allen JF and Raven JA (1996) Free-radical-induced mutationsvs. redox regulation: Costs and benefits ofgenes in organelles.J Mol Evol 42: 482-492

Anning T, MacIntyre HI., Pratt S, Sammes PJ, Gibb Sand GciderRJ (2000) Photoacclimation in the marine diatom Skeletonemacostatum. Limnol Oceanogr45: 1807-1817

Axelsson I., Larssen C and Ryberg H (1999) Affinity, capacityand oxygen sensitivity of two different mechanisms forbicarbonate utilization in Ulva lactuca L. (Chlorophyta). PlantCell Environ 22: 969-978

Badger MR, Andrews TJ, Whitney SM, Ludwig M, YellowleesDC, Leggat Wand Price GO (1998) The diversity andcoevolution of Rubisco, plastids, pyrenoids, and chloroplast-based COrconcentrating mechanisms in algae. Can J Bot 76:1052 1071

Badger MR, Hanson 0 and Price GO (2002) Evolution anddiversity ofCO2 concentrating mechanisms in cyanobacteria.Funct Plant Bioi 29: 161-173

Beardall J (1991) Effects of photon flux density on the COrconcentrating mechanism of the cyanobacterium Anabaenavariabilis. J Plankton Res 13 (suppl): 133-146

Bibby TS, Nield J and Barber J (200Ia) Iron deficiency inducesthe formation of an antenna ring around trimeric Photo systemI in cyanobacteria. Nature 412: 743-745

Bibby TS, Nield J, Partensky F and Barber J (200 1b)Oxyphotobacteria-antenna ring around Photosystem I. Nature413: 590.

Bjerrum CJ and Canfield DE (2002) Ocean productivity beforeabout 1.6 Gyr ago limited by phosphorus absorption on to ironoxides. Nature 417: 159-162.

Bjorkman0 (1981) Responses to different quantum flux densities.In: Lange 01., Nobel PS, Osmond CI3 and Ziegler H (eds)Physiological Plant Ecology. Encyclopedia of Plant Physiology,NS, Vol 12A, pp 57-107. Springer, Berlin

Boekema EJ, Hifncy A, Yakushewska AE, Piotrowski M,Keegstra W, Berry S, Michel KP, Pistorius EK and Kruip J(2001) A giant chlorophyll-protein complex induced by iron

deficiency in cyanobacteria. Nature 412: 745-748Bricaud A and Morel A (1986) Light attenuation and scatteringby phytoplankton cells: A theoretical modelling. Applied Optics25: 571-578

Bouman HA, Platt T, Kraay GW, Sathycndranath S and IrwinBD (2000) Bio-optical properties of the subtropical NorthAtlantic. I. Vertical variability. Mar Ecol Progr Ser 200: 3-18

Bricaud A, Allali K, Morel R, Marie D, Veldhuis MJW, PartenskyFand Vaulot 0 (1999) Divinyl chlorophyll a-specific absorptioncoefficients and absorption efficiency factors for Prochloro-coccus marinus: Kinetics ofphoto ace Iimation. Mar Ecol ProgrSer188:2132

Bunt JS (1965) Measurement of photosynthesis and respirationin a marine diatom with mass spectrometer and with C14.:\ature 207: 1373-1375

Campbell I., Nolla HA and Vaulot 0 1994 The importance ofProchlorococcus to community structure in the central NorthPacific Ocean. Limnol Oceanogr 39: 954-961

Canfield DE and Teske A (1996) Late Proterozoic rise inatmospheric oxygen concentration inferred from phylogeneticand sulphur-isotope studies. Nature 382: 127-132

Chadd HE, Newman J, Mann NH and Carr NG (1996)Identification of iron superoxidc dismutase and copper/zincsuperoxide dismutase enzyme activity within the marinecyanobacterium Synechococcus sp. WH 8803. FEMS MicrobiolLett 131: 161-165

Cocke II CS (2000) The ultraviolet history of the terrestrialplanets-implications for biological evolution. Planetary SpaceSci48: 203-214

Cote B and Platt T (1983) Day-to-day variations in the spring-summer photosynthetic parameters of coastal marine phyto-plankton. Limnol Oceanogr 28: 320-344

Crossett RN, Drew EA and Larkum AWD (1965) Chromaticadaptation in benthic marine algae. Nature 207: 547-548

Cullen J and Lewis MR (1988) The kinetics of algal photo-adaptation in the context ofvertical mixing. J Plankton Res 10:1039-1063

Davey MS and Geider RJ (2001) Impact of iron limitation on thephotosynthetic apparatus of the diatom Chaetoceros muelleri(Bacillariophyceae), J Phycol37: 987-1000

Demmig-Adams B and Adams WW III (1992) Photoprotectiveand other responses of plants to high light stress. Annu RevPlant Physiol Plant Mol BioI 43: 549~626

Dring MJ (1981) Chromatic adaptation of photosynthesis inmarine benthic algae: An examination of its significance usinga theoretical model. Limnol Oceanogr 26: 271-284

Dring MJ (1982) The Biology ofMarine Plants. Edward Amold,London

Dubinsky Z, Falkowski PO andWyman K (1986) Light harvestingand utilization in phytoplankton. Plant Cell Physiol27: 1335-1349

Engelmann TW (1983) Farbe und Assimilation. BotanischcsZeitung 41: 1-29

Erdncr DL and Anderson OM (1999) Ferredoxin and flavodoxinas biochemical indicators of iron limitation during open-oceaniron enrichment. Limnol Occanogr44: 1609-1615

Erdner 01., Price NM, Doucette GJ, Peleato ML and AndersonDH (1999) Characterization of ferredoxin and flavodoxin asmarkers of Fe limitation in marine phytoplankton. Mar EcolProgr Ser 184: 43-53

Escoboulos J-M, Loma M, LaRoche J and Falkowski PG (1995)

410

Light regulation of cab gene transcription is signalled by theredox state ofthe plastoquinone pool. Proc Natl Acad Sci USA92: 10237-10249

Falkowski PG and Raven JA (1997) Aquatic Photosynthesis.Blackwell Science, Malden

Falkowski PG and Dubinsky Z (1980) Light-shade adaptation ofStylophora pistillata, a hermatypic coral from thc Gulf ofEilat. Nature 289: 172-174

Falkowski PG, Dubinsky Z and Wyman K (1985) Growth-irradiance relationships in phytoplankton. Limnol Occanogr30: 311-321

Finazzi G, Furia A, Barbagallo RP and Forti G (1999) Statetransitions, cyclic and linear electron transport and photo-phosphorylation in Chlamydomonas reinhardtii. BiochimBiophys Acta 1413: 117-129

Flameling IA and Kromkamp J (1997) Photoacclimation ofScenedesmus protuberans (Chlorophyceae) to fluctuating PPFDsimulating vertical mixing. J Plankton Res 19: 1011-1024

Flynn KJ, Fasham MJR and Hipkin CR (1997) Modeling theinteractions between ammonium and nitrate uptake in marinephytoplankton. Phil Trans Roy Soc London 352: 1625-1645

Flynn KJ and Hipkin CR (1999) Interactions between iron, light,ammonium and nitrate; insights from the construction of adynamic model of algal physiology. J Phycol 35: 1171-1190

Flynn KJ, Marchall Hand Geider RJ (200 I) A comparison oftwoN-irradiance models of phytoplankton growth. LimnolOccanogr46: 1794-1802.

Fork DC, Herbert SK and Malkin S (1991) Light energydistribution in the brown alga Macrocystis pyrifera (giantkelp). Plant PhysioI95:731-739

Forster 13, Osmond CB and Boynton JE (2001) Very high lightresistant mutants of Chlamydomonas reinhardtii: Responsesof Photosystcm II, non-photochemical quenching andxanthophyll pigments to light and CO 2, Photosynth Res 67: S-IS

Franklin LA and Badger MR (2001) A comparison ofphotosynthetic electron transport rates in macroalgae measuredby pulse amplitude modulated chlorophyll fluorometry andmass spectrometry. J Phycol37: 756-767

Franklin LA and Forster RM (1997) The changing irradianceenvironment: Consequences for marine macrophyte physi-ology, productivity and ecology. Eur J Phycol 32: 207-232

Franklin LA and Larkum AWD (1997) Multiple strategies for ahigh light existence in a tropical marine macroalga. PhotosynthRes 53: 149-159

Franklin LA, Seaton GGR, Lovelock CE and Larkum AWD(1996) Photoinhibition ofphotosynthcsis on a coral reef. PlantCell Environm 19: 825-836

Gcidcr RJ (1987) Light and temperature dependence of thecarbon to chlorophyll ratio in microalgae and cyanobacteria:Implications for physiology and growth of phytoplankton.New Phytol 106: 1-34

Geidcr RJ and La Roche J (1994) The role ofiron in phytoplanktonphotosynthesis, and the potential for iron-limitation ofprimaryproductivity in the sea. Plant Cell Environm 39: 275-301

Geider RJ and La Roche J (2002) Redfield revisited: VariabilityofC:N:P in marine microalgae and its biochemical basis. EurJ Phycol 37: 1 17

Geider RJ, McIntyre HL and Kana TM (1996) A dynamic modelofphotoadaptation in phytoplankton. Limnol Oceancgr 41: I--IS

John A. Raven and Richard J. Geider

Geider RJ, Maclntyre HL and Kana TM (1998) A dynamicregulatory model of phytoplanktonic acclimation to light,nutrients, and temperature. Limnol Oceanogr 43: 679 -684

Gilstad M, Johnsen G and Sakshaug E (1993) Photosyntheticparameters, pigment composition and respiration rates of themarine diatom Skeletonema costatum grown in continuouslight and a 12: 12 h light-dark cycle. J Plankton Res IS: 939-951

Goerieke R, Olson RJ and Shalapyonok A (2000) A novel nichefor Prochlorococcus sp. in low-light suboxic environments inthe Arabian sea and the eastern tropical North Pacific. Deep-Sea Res I 47: 1183-1205.

Gocrickc R and Repeta D (1993) Chlorophylls a and banddivinyl ehlorophylls a and b in the open subtropical NorthAtlantic Ocean. Mar Ecol Prog Ser 101: 307-313.

Goericke Rand Wclschmcycr NA (1993) Prochlorophytepicoplankton contribute significantly to biomass and prodnc-tivity in the Sargasso Sea. Deep-Sea Res I 40: 2283-2294.

Goss R, Bohme K and Wilhelm C (1998) Thc xanthophyll cycleof Mantoniella squamata converts violoxanthin intoantheraxanthin but not to zeaxanthin: Consequences for themechanism ofenhanced non-photochemical energy dissipation.Planta 205: 613-621

Graziano LM, Geider RJ, Li WKW and Olaizola M (1996)Nitrogen limitation ofNorth Atlantic phytoplankton: Analysisofphysiological condition in nutrient enrichment experiments.Aqu Microbial Ecol II: 53-64

Harvey WI! (1836) Algae. In: Mackay JT (ed) Flora HibemicaPart 3, pp 157-257. Curry and Company, Dublin

Hess WR, Rocap G, Ting CS, Larimer F, Stilwagen S, LamerdinJ and Chisholm SW (2001) The photosynthetic apparatus ofProchlorococcus: Insights through comparative genomics.Photosynth Res 70: 53-71

Hope AB (2000) Electron transfers amongst cytochrome f,plastocyanin and Photosystem I: kinetics and mechanisms.Biochim Biophys Acta 1456: 5-26

Kain J:vl (1989) Thc seasons in the subtidal. Br PhycolJ24: 203-215

Kana TM (1992) Relationship between photosynthetic oxygencycling and carbon assimilation in Synechococcus WH 7803(Cyanophyta). J Phycol 28: 304-308

Kana TM, Geider RJ and Critchley C (1997) Dynamic balancetheory of pigment regulation in microalgae by multipleenvironmental factors. New Phytol 137: 629-638

Kaneko T, Sato S, Kotani H., Tanaka A., Asamizu E, NakamuraY, Miyajama N, HirosawaM, Sugiura M, Sasamoto S, KimuraT, Hosouchi T, Matsuno A, Muraki N, Naruo K, Okumura S,Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M,Yasuda M and Tabata S (1996) Sequence analysis of thegenome of the unicellular cyanobacterium Synechocystis sp.strain PCC 6803. II. Sequence determination of the entiregenome and assignment of potential protein-coding genes.DNA Res 3: 109-136

Kiefer DA and Mitchell BG (1983) A simple, steady-statedescription of phytoplankton growth based on the absorptioncross-section and quantum efficiency. Limnol Occanogr 28:770-776

Kirk JTO (1994) Light and Photosynthesis in Aquatic Ecosystems,Second Edition. Cambridge University Press, Cambridge

Kromkamp J and Limbeck M (1993) Effect ofshort-term variationin irradiance on light harvesting and photosynthesis of the

Chapter 17 Adaptation, Acclimation and Regulation 411

marine diatom Skeletonema costatum: A laboratory studysimulating vertical mixing. I Gen Microbiol 139: 2277-2284

Kubler IE and Raven IA (1995) The interactions betweeninorganic carbon supply and light supply inPalmariapalmata.I Phycol31: 369-375

Kyewalyanga MN, Platt T, Sathyendranath S, Lutz VA andStuart V (1998) Seasonal variations in physiological parametersof plankton in the North Atlantic. I Plankton Res 20: 17-42

Larkum T and Howe CI (1997) Molecular aspects of light-harvesting processes in algae. Adv Bot Res 27: 257-330

Larkum AWD, Drew EA and Crossett RN (1967) The verticaldistribution of attached marine algae in Malta, I Eco155: 361-371

La Roche J, Murray H, Orellana \1 and Newton J (1995)Flavodoxin expression as an indicator of iron limitation inmarine diatoms. J Phycol 31: 520-530

La Roche J, Boyd PW, MeKay RML and Geider RJ (1996)Flavodoxin as an in situ marker for iron stress in phytoplankton.Nature 382: 802-805

Laskar J, Joutcl F and Robutel P (1993) Stabilization of theEarth's obliquity by the moon. Nature 361: 615 617

Laws EA and Bannister '1''1' (1980) Nutrient- and light-limitationof Thalassiosira fiuviatilis in continuous culture, withimplications for phytoplankton growth in the ocean. LimnolOceanogr 25: 457-473.

Li LA, Zianni MR and Tabita FR (1999) Inactivation of thernonocistronic rca gene in Anabaena variabilis suggest aphysiological ribulose bisphosphate carboxylase oxygenaseactivasc-likc function in hctcrocystous cyanobacteria. PlantMol I3ioI40: 467-478

Littler MM and Littler DS (1994) Algenwachstum in ozeanischenTiefer. Unsere Zeit (24 Jahr, 1944) Nr 6: 330-335

Littler MM, Littler DS, Blair S and Norris N (1985) Deepestknown plant life discovered on an uncharted seamount. Science227: 57 59

Lohr M and Wilhelm C (1999) Algae displaying the diadino-xanthin cycle also possess the violoxanthin cycle. Proc NatlAcad Sci USA 96: 8784-8798

Lomas MW and Glibert PM (1999) Temperature regulation ofnitrate uptake: A novel hypothesis about nitrate uptake andreduction in cool-water diatoms. Limnol Oceanogr 44: 556-572

Long SP Humphries S and Falkowski PG (1994) Photoinhibitionofphotosynthesis in nature. Annu Rev Plant Physiol Plant MolBio145: 633-662

Luning K (1993) Environmental and internal control of seasonalgrowth in seaweeds. Hydrobiologia 260/261: 1-4

MacIntyre HL, Kana 'I'M and Geider RJ (2000) The effect ofwater motion on short-term rates of photosynthesis by marinephytoplankton. Trends Plant Sci 5: 12-17

Macintyre HL, Kara TM, Anning 'I' and Geider RJ (2002)Photoacclimation ofphotosynthesis irradiance response curvesand photosynthetic pigments in microalgae and cyanobacteria.J Phycol 38: 17-38

McKay RM, La Roche J, Yakumin AF, Durnford DG and GciderRJ (1999) Accumulation of ferredoxin and flavodoxin in amarine diatom in response to Fe. J Phycol 35: 510-519

Maxwell DP, Laudenbach DE and Huner NPA (1995) Redoxregulation of light-harvesting complex II and cab messenger-RNA abundance in Dunaliella salina. Plant Physiol l 09: 787-795

Mazel D and Marliere P (1989) Adaptive eradication ofmethioneand cysteine from cyanobacterial light-harvesting proteins.Nature 341: 245-248

Mitchell BG and Kiefer DA (1988) Variability in pigment specificparticulate fluorescence and absorption in the northeasternPacific Ocean. Deep-Sea Res 35: 665-689

Moison 'I'A and Mitchell I3G (1999) Photophysiologicalacclimation of Phaeocystis antarctica Karsten under lightlimitation. Limnol Oeeanogr 44: 247-258

Moore LR and Chisholm SW (1999) Photophysiology of themarine cyanobacteriumProchlorococcus: Eeotypic differencesamong cultured strains. Limnol Oceanogr 44: 628-638

Neilsen MV and Sakshaug E (1993) Photophysiologieal studiesof Skeletonema costatum adapted to spectrally different lightregimes. Limnol Oceanogr 38: 1576-1581

Ornata T, Price GD, Badger MR, Okamura M, Gohta SandOgawa 'I' (1999) Identification of an ATP-binding cassettetransporter involved in bicarbonate uptake in the eyano-baeteriumSynechococcus sp. strain pee7942. Proc Natl AcadSci USA 96: 13571--13576

OsmondCB and Grace SC (1995) Perspectives on photo inhibitionand photorespiration in the field-quintessential inefficienciesofthe light and dark reactions ofphotosynthesis. J Exp Bot 46:1351 1362

Pfannsehmidt '1', Nilsson A and Allen IF (1999) Photosyntheticcontrol of chloroplast gene expression. Nature 397: 625-628

Platt T, Subba-Rao DV, Smith JC, Li WKW, Iravin B, HorneEPW and Sameoto DD (1983) Photosynthetically competentphytoplankton from the aphotic zone of the deep ocean. MarEcol Progr Ser 10: 105 110

Platt '1', Harrison WG, Irwin B, Horne EP and Gallegoes CL(1982) Photosynthesis and photoadaptation of marinephytoplankton in the Arctic. Deep-Sea Res 29: 1159-1170

Ploug H, Stolte W and Jorgensen BB (I 999a) Diffusive boundarylayers of the colony-forming plankton alga Phaeocystis sp.-implication for nutrient uptake and cellular growth. LimnolOceanogr44: 1959-1967

Ploug H, Stolte W, Epping EHG and Jorgensen I3I3 (1999b)Diffusive boundary layers, photosynthesis and respiration ofthe colony-forming plankton alga, Phaeocystis sp. LimnolOeeanogr44: 1949-1958

Poole LJ and Raven JA (1997) The biology of Enteromorpha.Adv Bot Res 12: 1-148

Potts M (1999) Mechanisms of desiccation tolerance incyanobacteria. Eur J Phycol34: 319-328

Raven JA (1984a) Energetics and Transport in Aquatic Plants.AR Liss, New York

Raven JA (I 984b) A cost-benefit analysis of photon absorptionby photosynthetic unicells. New Phytol 98: 593-625

Raven JA (1986) Physiological consequences ofextremely smallsize for autotrophic organisms in the sea. In: Platt 'I' and LiWKW (cds) Photosynthetic Pieoplankton, pp 1-70. Can BullFisheries Aquat Sci 24

Raven JA (1990) Sensing pH? Plant Cell Environm 13: 721-729Raven JA (1991) Physiology of inorganic C acquisition andimplications for resource use efficiency by marine phyto-plankton: relation to increased CO 2 and temperature. PlantCell Environm 14: 779-794

Raven JA (1993) The evolution ofvascular land plants in relationto quantitative functioning ofdead water-conducting cells andstomata. BioI Rev 68: 337-363

412

Raven JA (1996) The bigger the fewer: Size, taxonomic diversityand the range of pigments in marine phototrophs. J Mar BioiAssoe UK 76: 211-217

Raven JA (1997) Inorganic carbon acquisition by marineautotrophs. Adv Bot Res 27: 85-209

Raven JA (1998) Small is beautiful. The pieophytoplankton.FunctEcol 12: 503-513

Raven JA (1999) Picophytoplankton. Progr Phycol Res 13 : 33-106

Raven JA (2000) Land plant biochemistry. Phil Trans Roy SocLondon B 355: 833 846

Raven JA and Gcidcr RJ (1988) Temperature and algal growth.New Phytol 110: 441-461Raven JA and Kubler JE (2002) New light on the scaling ofmetabolic rate with the size of algae. J Phycol38: 11-16.

Raven JA, Johnston AM and Surif M bin (1989) Thcphotosynthetic apparatus as a phyletic character.In: Green JC,Leadheater BSC and DiverWI (eds) Problems andPerspectives.The Chromophyte Algae, pp 63-84. Clarendon Press, Oxford

Raven JA, Johnston AM, Kubler J and Parsons R (1994) Theinlluence of natural and experimental high 02 concentrationson 0Tevolving photolithotrophs. Biol Rev 69: 61-94

Raven JA, Kubler JE, Johnston AM, Poole LJ, Taylor RandMcInroy SG (1998) Oxygen-insensitive growth of algae withand without COTconcentrating mechanisms: In: Garab G (cd)Photosynthesis: Mechanisms and Effects, Vol V, pp 3331-3337. Kluwer Academic Publishers, Dordrccht

Raven JA, Evans MCW and Korb RE (1999) The role of tracemetals in photosynthetic electron transport in 0Tcvolvingorganisms. Photosynth Res 60: 111-149

Raven JA, Kubler JE and Beardall J (2000) Put out the light, andthen put out the light. J Mar Bioi Assoc UK 80: 1-25

Richardson KR, Beardall J and Raven JA (1983) Adaptation ofunicellular algae to irradiance: An analysis of strategies. NewPhytol 361: 249-251

Rowan KS (1989) Photosynthetic Pigments in Algae. CambridgeUniversity Press, Cambridge

John A. Raven and Richard J. Geider

Salih A, Larkum A, Cox G, Kuhl M and Hocgh-Guldberg °(2000) Fluorescent pigments in corals arc photoprotective.Nature 408: 850-853.

Shuter B (1979) Amodel of physiological adaptation inunicellularalgae. J Theoret Bioi 78: 519-552

Subramaniam A, Carpenter EJ, Karentz D and Falkowski PG(1999) Bio-optical properties of the marine diazotrophiecyanobacteria Trichodesmium spp. I. Absorption and photo-synthetic action spectra. Limnol Oceanogr 44: 608-617

Sukenik A, Bennett J and Falkowski PG (1987) Light-saturatedphotosynthesis-limitation by electron transport or carbon-fixation? Biochim Biophys Acta 891: 205-215

Ting CS, Rocalp G, King J and Chisholm SW (2002)Cyanobacterial photosynthesis in the oceans: The origins andsignificance of divergent light-harvesting strategies. TrendsMicrobiol 10: 134-142

Ursi S, Pedersen M, Plastino E and Snoeijs P (2003) Intraspecificvariation of photosynthesis, respiration and photoprotectivecarotenoids in Gracilaria birdae Gracilariales (Rhodophyta).Mar Bioi 142: 997-1007

van den Hock C, Mann DG and Jahns HM (1995) Algae. AnIntroduction to Phycology. Cambridge University Press,Cambridge

Walker JGC, Klein C, Schidlowski M, SehopfJW, Stevenson DJand Walker MR (1983) Environmental evolution of theArchean-early Proterozoic Earth. In: Schopf JW (ed) Earth'sEarliest Biosphere, pp 260-290. Princeton University Press,Princeton

White 0, Eisen JA, Heidelberg JF, Hickey EK, Peterson JD,Dodson RJ, Haft DB, Gwinn ML, Nelson WC, RichardsonDL, Moffat KS, Qin H, Jiang L, Pamphile W, Crosby M, ShenM,Vamathalen JJ,Lam P,McDonald L, Utterbeek T,ZalewskiC, Makarova KS, Aravind L, Daly MJ, Minton KW,Fleischmann RD, Ketchum KA, NelsonKE, Salzberg S, SmithHO, Venter JC and Fraser CM (1999) Genome sequence of theradioresistant bacterium Deinococcus radiodurans Rl. Science286: 1571-1577