REGULAR PAPER

The origin of the temperature-induced fluorescence fluctuationin Spirulina platensis: temperature-sensitive mobilityof PQ molecules

Heng Li Æ Shuzhen Yang Æ Jie Xie Æ Juanjuan Feng ÆYandao Gong Æ Jingquan Zhao

Received: 3 July 2006 / Accepted: 18 June 2007 / Published online: 19 July 2007

� Springer Science+Business Media B.V. 2007

Abstract Temperature effects on state transitions have

been studied in the cyanobacterium Spirulina platensis. At

lower temperatures the time to reach completion took

longer and the extent of the state transitions was larger.

Effects were limited to the temperature range below the

phase transition temperature of the membrane lipids. In the

presence of the artificial electron acceptor phenyl-1,4-

benzoquinone (PBQ) state transitions became completely

temperature-independent. State transitions induced by a

change in the light climate or in darkness by a switch from

aerobic to anaerobic conditions responded similar to tem-

perature; the occurrence of state transitions solely by a

change of the temperature has been excluded. Our con-

clusion is that the temperature-dependent mobility of

plastoquinone molecules in the thylakoid membranes is the

intrinsic cause of temperature effects on state transitions.

Keywords Electron transfer � Fluorescence fluctuation �Mobility of plastoquinone molecules � State transition �Temperature

Abbreviations

APC Allophycocyanin

C-PC C-phycocyanin

Cyt b6 f Cytochrome b6 f

DCMU 3-(3, 4-dichlorophenyl)-1, 1-dimethylurea

PBS Phycobilisome

PBQ Phenyl-1,4-benzoquinone

PSI Photosystem I

PSII Photosystem II

PQH2 Plastoquinol

PQ Plastoquinone

RT Room temperature (25�C)

TPT Phase transition temperature

Introduction

Changes in the relative fluorescence emission of the three

photosynthetic functional entities, phycobilisome (PBS),

photosystem II (PSII) and photosystem I (PSI) are adequate

to monitor the rapid physiological response of cyanobac-

terial cells to a special physical or chemical ‘‘stimulus’’. If

suddenly exposed to a light condition specially favouring

PSI or PSII, the photosynthetic machinery rebalances the

excitation energy distribution between the two photosys-

tems in order to maximize the photosynthetic efficiency

(Allen 2003). Such an adaptation seen as fluctuation in

fluorescence is called ‘‘light state transition’’ (Bonaventura

and Myers 1969; Murata 1969; Fork and Satoh 1983).

Study of the light state transitions in cyanobacteria have

not only contributed to improved understanding of the

phenomenon itself; it also supported extension of the

knowledge about the photosynthetic and respiratory elec-

tron transport pathways that share components including

the plastoquinone (PQ) pool and cytochrome b6f (Cyt b6f)

(Mullineaux and Allen 1986; Scherer 1990).

H. Li � S. Yang � J. Xie � J. Zhao (&)

Beijing National Laboratory for Molecular Sciences (BNLMS),

Photochemistry Laboratory, Institute of Chemistry,

Chinese Academy of Sciences, Beijing 100080, P.R. China

e-mail: zhaojq@iccas.ac.cn

J. Feng � Y. Gong

State Key Laboratory of Biomembrane and Membrane

Biotechnology, Department of Biological Sciences and

Biotechnology, Tsinghua University, Beijing 100084, P.R. China

123

Photosynth Res (2007) 94:59–65

DOI 10.1007/s11120-007-9214-9

A state transition can be created by selective excitation

of PSII or PSI (Mullineaux and Allen 1990). State 1 cor-

responds to an oxidized PQ pool and state 2 to a reduced

PQ pool. In cyanobacterium cells, the photosynthetic and

respiratory electron chains are intersected at the PQ pool,

therefore a light state 2 could also be produced by dark

adaptation (Mullineaux and Allen 1986). Temperature-re-

lated effects on the fluorescence emission in cyanobacteria

have earlier been studied under dark conditions (Manodori

and Melis 1985; Li et al. 2001, 2003). Li et al. have since

found a pattern of changes in state transitions that inde-

pendently of being induced by light or in darkness when

the temperature was changed from RT to 0�C; altered PBS

mobility on the thylakoid membrane was suggested as a

cause (Li et al. 2004). However, in contrast to this pro-

posal, Sarcina et al. have reported that PBS mobility is

temperature-independent from 10�C to 30�C, which con-

clusion has been based on observations of fluorescence

recovery after photobleaching (FRAP) (Sarcina et al.

2001). Further aspects of temperature effects in cyano-

bacteria relate to the phase transition temperature (TPT) of

the membrane lipids, which are typically observed well

below the growth temperature (Murata 1989). In this study

light-induced state transitions have been studied at differ-

ent temperatures to reveal the actual cause for the effects of

temperature on the kinetics of state transitions and their

mechanism of function behind.

Materials and methods

Culture and growth conditions

Spirulina platensis was originally obtained from the Insti-

tute of Botany, the Chinese academy of Sciences. Cells

were cultured in the Zarrouk medium (pH 9.0) (Zarrouk

1966) at 28�C in a 1 l bottle bubbled with air under con-

tinuous illumination at a photon flux density of 50 lmol

m–2 s–1 with white fluorescent light. Ten-day-old cultures

were harvested by centrifugation, washed and re-suspended

in fresh growth medium.

Spectral measurements

Absorption spectra were recorded on a UV-1601 ultra-vis

spectrophotometer (Shimadzu, Japan). Fluorescence emis-

sion spectra were obtained at 77 K on an F4500 spectro-

fluorimeter (Hitachi, Japan) with a chlorophyll a

concentration of 5 lg ml–1 estimated by the absorbance at

665 nm in methanol extracts (Porra et al. 1989). For 77 K

fluorescence measurements, samples were rapidly frozen

into liquid nitrogen. The excitation and emission slit widths

were set at 5 nm.

Methods for inducing state transitions

For light-induced state transition, the light state 1 was in-

duced by blue light (Ditric optics 460 nm short-pass filter)

at 100 lmol m–2 s–1 and the state 2 by orange light (via a

Ditric optics 580 nm long-pass and a 600 nm short-pass

filter) at 20 lmol m–2 s–1 (Mullineaux and Allen 1990).

Conditions for setting an ‘‘extreme’’ state 1 by blue light in

the presence of DCMU and an ‘‘extreme’’ state 2 induced

by dark adaptation under anaerobic condition were

according to Bruce et al. (1989). A circulating water bath

was used for keeping the cells at a certain temperature. To

detect the temperature effect on the light-induced transition

from state 2 (or state 1) to state 1 (or state 2), dark-adapted

cells were pre-illuminated by orange (blue) light for

20 min at a certain temperature and then a sample was

taken for a 77 K fluorescence spectrum; illumination of the

sample was continued in blue (orange) light for another

20 min at the same temperature, again taking a sample for

a 77 K spectrum. For dark-induced state transition, the

cells were dark-adapted at a selected temperature in

ambient air for 15 min before spectral measurements;

anaerobic samples (state 2) were prepared by bubbling with

Ar for 30 min in the dark. It has been reported that the

artificial quinone phenyl-1,4-benzoquinone (PBQ) can

independently induce a state 1 (Mao et al. 2002) by its

ability to accept electrons from Q�A directly, which causes

efficient oxidation of the PQ pool (Petrouleas and Diner

1987; Satoh et al. 1992; Tyystjarvi et al. 1999). Accord-

ingly, fluorescence changes have been induced in the

presence of PBQ, by dark-adapting cells for 30 min at each

temperature and subsequent addition of 1 mM PBQ under

dark conditions.

Oxygen electrode measurements

Rates of oxygen evolution by intact cells were measured

with a Clark-type oxygen electrode (Hansatech oxygraph)

in the absence and presence of 1 mM PBQ. The chloro-

phyll a concentration was adjusted to 15 lg ml–1 and a

light intensity of 1000 lmol m–2 s–1 was used. Air-satu-

rated and temperature-equilibrated water was used to cal-

ibrate the electrode at each temperature. Photosynthetic

oxygen-evolution rates at a range of temperatures also

served to determine the phase transition temperature of the

membrane lipids (TPT) with an Arrhenius plot of photo-

synthetic oxygen evolution versus temperature (Murata

et al. 1984).

60 Photosynth Res (2007) 94:59–65

123

Results

The temperature effects under various light conditions

Figure 1 shows the 77 K fluorescence emission spectra as

well as the derived difference spectra for intact cells of

Spirulina platensis under various light conditions at both

RT and at 0�C. Four partially resolved peaks have been

ascribed to C-PC (648 nm), APC (660 nm), PSII (693 nm)

and PSI (728 nm), respectively (Rakhimberdieva et al.

2001; Li et al. 2004). The results demonstrated the exis-

tence of temperature-related effects on light-induced state

transitions (Fig. 1a–d). The cells illuminated by blue light

at 0�C produced a more extended state 1 than seen at RT

(Fig. 1a, b) while state 2 was larger at 0�C in orange light

(Fig. 1c, d). These results indicate that the extent of state

transitions is more pronounced at 0�C. However, this

change in fluorescence emission appeared completely ab-

sent if cells were illuminated by just energy-balanced

culture light (Fig. 1e, f). This demonstrates that a change in

the temperature as such cannot induce a state transition

independently.

How does the temperature affect the state transitions?

To determine how a state transition is affected by tem-

perature, kinetic plots of the rate of change in emission

ratios of PSII to PSI (F693/F728) resulting from a light-

induced state transition have been studied at a range of

temperatures (Fig. 2). The FPSII/FPSI ratio has long been

used as an indicator to character a light state (Bruce et al.

1989). The data clearly demonstrate that the time for

completion of a state transition takes up to 12 times longer

at 0�C than at 20�C on the one hand, and that the amplitude

of the change is more than 30% larger at low temperature

than at RT on the other hand. These temperature effects are

not linear, as is demonstrated by a clear break in the curves

that plot FPSII/FPSI for the blue-light-induced state 1 and

orange-light-induced state 2 to temperature (Fig. 3 closed

a b

c d

e f

Fig. 1 Fluorescence emission spectra recorded at 77 K for intact

cells illuminated by blue light (a), orange light (c), and culture light

(e). The solid lines represent data for cells illuminated at RT and

dashed one for cells illuminated at 0�C, respectively. Difference

spectra for cells illuminated at 0�C minus those illuminated at RT for

each experimental condition (b, d and f). The spectra were excited at

580 nm and normalized at 707 nm

a b

Fig. 2 Time course of FPSII/FPSI change during light-induced state

transitions for a series of temperatures. Orange-light-induced state 2

to blue-light-induced state 1(a); ibid for state 1 to state 2(b)

Photosynth Res (2007) 94:59–65 61

123

squares and open squares). For Spirulina platensis in our

growth conditions the results in Figs. 2 and 3 thus dem-

onstrate that state transitions can be completed at any

temperature, even at 0�C and also that state transitions are

temperature-independent above 18�C. The temperature

effects have in principle been observed regardless of the

state transitions being induced by a change in the light

climate or in darkness, though the amplitude of the change

in the light-induced case (Fig. 3 closed squares and open

squares) proved smaller than in the dark respiratory change

(Fig. 3 circles) realized state transition.

In fact, the extent of state transitions actually can vary

substantially between conditions as is shown for a sequence

ranging from an ‘‘extreme’’ state 1 induced by blue light in

the presence of DCMU to an ‘‘extreme’’ state 2 induced by

dark adaptation under anaerobic conditions and interme-

diate cases of a blue-light induced state 1, an orange-light-

induced state 2 and a state induced by dark adaptation

under aerobic conditions at RT. Interestingly, the extent of

the state transition for dark-adapted cells in aerobiosis at

0�C is nearly the same as the one under anaerobic condition

at RT, suggesting that the ‘‘extreme’’ state 2 may be

achieved by lowering the temperature to 0�C (Fig. 4).

Why the state transitions are temperature-dependent?

From Fig. 3, it can be seen that the apparent breaking point

of the plots appears at around 18�C, which is 10�C lower

than the culture temperature and may coincide with the

phase transition temperature (TPT) of the membrane lipids

in Spirulina platensis (Murata 1989). To determine the

phase transition temperature of the membrane lipids (TPT)

in Spirulina platensis, the relation between photosynthetic

oxygen evolution and temperature was determined. From

data shown by the solid line in Fig. 5 TPT value of 18�C

was derived, which correlates nicely with the breaking

point of the three lines in Fig. 3 and indicates that the effect

of temperature on state transitions originates from factors

that are susceptible to phase transition of the membrane

lipids.

Phenyl-1,4-benzoquinone (PBQ) molecules were added

as intercepting electron acceptors which eliminates the

contribution of temperature-dependent PQ-molecule

mobility for electron transfer to proceed, the results are

shown in Fig. 6a. Compared to the dark-induced state 2,

adding excessive PBQ molecules to the dark-adapted cells

led to an increase in PSII fluorescence but decrease in the

PSI, indicating a state transition from state 2 into state 1. It

was confirmed that the PBQ-induced state could hardly be

changed by blue- or orange-light illumination (data not

shown), suggesting that the cells are locked in an ‘‘ex-

treme’’ state 1. At the same time, the fluorescence from the

phycobilisomes apparently increased. Figure 6b demon-

strates that the state transition from the dark-induced state 2

to PBQ-induced state 1 is completely temperature-inde-

pendent from RT to 0�C (Fig. 6b open squares). This

°

Fig. 3 Plots of the ratio of fluorescence from PSII and PSI FPSII/FPSI

as a function of temperature for some selected states. Blue-light-

induced state 1 (closed squares); orange-light-induced state 2 (opensquares); dark-induced state 2 (circles). For each temperature, the

mean of three independent measures is plotted with the standard

deviation (SD) denoted by error bars

°

Fig. 4 Dependence of the extent of state transitions on the inducing

conditions (details are given in the figure). The 77 K fluorescence

spectra were excited at 580 nm and normalized at 707 nm

°

°

Fig. 5 Arrhenius plot of photosynthetic oxygen evolution in Spiru-lina platensis. S, Control cell (solid lines); cells in the presence of

1 mM PBQ (dashed line)

62 Photosynth Res (2007) 94:59–65

123

supports that PQ mobility is the factor which is responsible

for the temperature effect.

The data in Fig. 6 fit well to the data of the oxygen

evolution experiment that has been presented in Fig. 5. The

oxygen-evolution rates of the cells in the presence of PBQ

molecules were next measured at a series of temperatures.

As shown in Table 1, the oxygen-evolution rates in the

presence of PBQ increased greatly at all tested tempera-

tures which are due to the more efficient electron transfer.

Especially, when the oxygen-evolution rates were nor-

malized to the value for the control at 30�C, a single-slope

plot of the oxygen-evolution rates to temperature was de-

rived (Fig. 5, dashed line); note that this coincided exactly

with the solid line above the TPT. This suggests that the

oxygen-evolution rates below TPT depend on two factors:

the linearly temperature-dependent activity of the oxygen-

evolution centres and the temperature-sensitive mobility of

PQ molecules, while the latter would be eliminated in the

presence of PBQ.

Discussion

It is well known that state transitions depend on the redox

state of the PQ pool (Mullineaux and Allen 1986), and also

that PQH2 molecules transport electrons in the lipid

membrane from the QB site of PSII to QO site of cyto-

chrome b6f (Cyt b6f) by diffusion (Tikhonov et al. 1980). It

has been proposed that the larger slope for the oxygen-

evolving rates at temperatures lower than TPT was due to

PQ molecule-related reactions and the impact of membrane

fluidity on PQ (Murata et al. 1975). This has been ex-

plained by the fact that membrane lipids undergo a phase

transition from liquid-crystalline to gel phase rendering

distinctive differences in diffusion coefficients for mem-

brane embedded molecules above and below the TPT of the

membranes (Murata et al. 1975). Therefore, observation of

a temperature-related breaking point for a given reaction

makes plausible that the diffusion of functional molecules

inside membranes is affected by temperature in the gel

phase.

Photosynthetic and respiratory electron chains intersect

at the PQ pool (Mullineaux and Allen 1986; Scherer 1990).

The similarity of the temperature effects observed in this

work for light- and dark-induced state transitions and also

the fact that the breaking point in the fluorescence-induc-

tion curve appeared at TPT has put focus on the role of the

PQ pool to explain the effects of temperature on state

transitions. Also, the fact that the phase transition tem-

perature is about 10�C lower in the current results than the

culture temperature, coincides nicely with the known

behaviour of the phase transition temperature (TPT) for the

membrane lipids in cyanobacteria (Murata 1989). Below

the TPT, the membrane lipids in the gel phase are less

mobile, which implies that the mobility of the PQ mole-

cules becomes lower. Lower mobility gives rise to a slower

transfer of electrons so an accumulation of reduced PQ

molecules in the PQ pool due to slow re-oxidation. Hence,

photosystems are sensing a more reduced PQ pool, which

has indeed been observed as a higher extent of state 2 under

illumination by orange light or in dark adaptation (Figs. 1c,

d, 3 open squares, circles). While under illumination by

blue light, the slower transfer of electrons from the QB site

to PQ molecule resulted in a more oxidized PQ pool and a

higher extent for state 1 (Figs. 1a, b, 3 closed squares).

However, under culture light only (Fig. 1e, f), the imbal-

ance in redox state was not observed, here the mobility of

just reduced PQH2 from QB to the PQ pool and that from

PQ pool to QO are likely both slowed down but in balance,

therefore the temperature effect was absent. It is concluded

a b

°

Fig. 6 77 K fluorescence emission spectra for a dark-adapted state 2

(a, solid line) to a PBQ-induced state 1 (a, dashed line); Plots of time

versus temperature for the transition from a dark-induced state 2 to a

blue light or PBQ-induced state 1(b)

Table 1 Rates of oxygen evolution under saturating light using cells in growth medium. (lmol of O2 (mg of chl)–1 h–1)

Temperature (�C) 30 27 25 23 20 16 14 12 10 8 6

Control 229 203 190 175 145 116 90.3 62.1 35.1 14.1 –

1 mM PBQ 986 886 815 740 626 514 461 370 293 234 172

Normalized 229 206 188 172 147 122 107 86.1 68.1 54.5 40.1

Normalized, the value for the cells in the presence of 1 mM PBQ were normalized to the value for the control at 30�C

Photosynth Res (2007) 94:59–65 63

123

that temperature as such cannot induce a state transition

independently; redox force exerted by change of light or

respiratory conditions is a prerequisite.

Use of artificial electron accepting PBQ molecules that

accept from Q�A and also oxidize any reduced PQ mole-

cules renders a fully oxidized PQ pool that thus fixes cells

in state 1. The change in fluorescence emission in Fig. 6a is

therefore taken as an indication of a state transition with

certainty no matter the unresolved questions about the

mode of action of PBQ. In the presence of PBQ, the

electrons are not transported by the mobile PQ molecules,

which explains the observed absence of the temperature

effect in the PBQ-induced state 1 transition no matter of

testing below or above the TPT. The significant increase in

fluorescence emission originating from the PBS relative to

the florescence emission from the photosystems can be

reasonably ascribed to a less-efficient energy transfer due

to detachment of the PBSs from the photosystems, very

similar to the glycerol-induced detachment of PBSs from

the thylakoid membranes. In our previous paper (Li et al.

2007), it was observed that glycerol could weaken the

hydrophobic interaction of not only PBS with the thylakoid

membrane but also in a PBS. In this case, the energetic

coupling not only of a PBS with the photosystems but also

of the components in a PBS would become weaker. Be-

sides as an electron acceptor, PBQ is also a lipophilic

compound so may act as glycerol similarly. Therefore, the

higher fluorescence for C-PC and APC than the terminal

emitters is understandable. However, playing a role of

weakening the hydrophobic interaction is not explosive. As

an electron acceptor, PBQ could accept the electron from

PSII so keep the PQ pool in oxidized state so the cells in

light state 1. Therefore, no matter the complexities induced

by PBQ, a well-known function of it is to keep the PQ pool

always in oxidized state, so certainly produced a light state

1. In this case, the electron transfer and the redox state of

PQ pool did not rely on the mobility of PQ molecules, so

the state transition did not rely on temperature. Further, the

relative difference between PSII and PSI fluorescence

could not be ascribed to a direct quenching of the Chl

fluorescence, for the PBS fluorescence would have been

synchronously quenched with the Chl fluorescence if the

energy transfer efficiency from PBSs to the photosystems

kept invariable after addition of PBQ. The fluorescence

change observed in Fig. 6a is a result of two effects caused

by PBQ: the state 2 to the state 1 transition and weakening

of the hydrophobic interaction.

In conclusion, the current work confirms that the tem-

perature effects on the light- and dark-induced state tran-

sitions are common and dual directional, low temperature

makes increase the extent of state 1 and state 2 even fur-

ther, respectively. A state transition can be achieved at any

tested temperatures, even at 0�C but much longer time to

complete. Moreover, the absence of temperature effects

under culture light implies that temperature cannot induce

the state transition independently but rather promotes the

extent of a state transition. The state transitions proved

temperature-independent above TPT but are linearly

dependent below that temperature. Notably, the tempera-

ture effect was absent in the dark-induced state 2 and in the

PBQ-induced state 1 transition in which case the necessity

of PQ mobility for electron transfer was eliminated; at the

same time, the plot of the oxygen-evolution rates to tem-

perature becomes a single-slope line in the presence of

PBQ. These results clearly demonstrate that the tempera-

ture-sensitive mobility of the PQ molecules in the mem-

brane lipids is the ‘‘intrinsic cause’’ of the temperature

effect on the state transitions in Spirulina platensis cells.

Acknowledgement This research project has been supported by the

National Natural Science Foundation of China (NSFC) by grants No.

30570422, 50221201 and 90306013.

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