Current Biology Vol 18 No 12R518

Dispatches

Diatom Signalling: Deadly Messages

How are populations of phytoplankton in the oceans regulated? Recent studiesare revealing the presence of complex cell–cell and intracellular signallingmechanisms that can lead to growth regulation and even programmed celldeath in response to abiotic stress and biotic interactions.

Colin Brownlee

Oceanic phytoplankton play a majorrole in the sequestration ofatmospheric CO2. The importance ofphysical factors in determiningphytoplankton growth and distributionpatterns have long beenacknowledged. Variations in the supplyof nutrients (most notably nitrogen,phosphorus, and iron) arising fromdifferences in ocean circulationpatterns, tidal fronts, and proximity toland-based nutrient sources underlyconsiderable geographic variabilityand seasonal growth. Under optimalconditions, certain phytoplanktonspecies can grow rapidly over verywide areas. This bloom-formingcapacity is typical of a number ofmarine prokaryotic and eukaryoticphytoplankton species, includingcyanobacteria, dinoflagellates,coccolithophores, and diatoms. Suchrapid phytoplankton growth can leadto nutrient limitation and, ultimately, tothe collapse of blooms. However, inrecent years, growth suppression bynutrient limitation has been shownto be only part of the story.

A number of studies have shownthat stress and nutrient limitationconditions may not only limit growthrate but also trigger mechanisms thatlead to controlled growth reductionand even cell death [1]. Moreover,biotic interactions also appear toplay an important role in regulatingphytoplankton growth in a number ofsystems [1]. It is now understood thatnutrient limitation and other abioticstress stimuli, such as light limitation,can initiate intracellular signallingpathways that cause cells to undergoprogrammed cell death (PCD) inboth eukaryotic and prokaryoticphytoplankton [2–4]. The occurrenceof PCD pathways in distantly relatedgroups, including prokaryotes,indicates that this process has deepevolutionary roots [2]. While PCD

has been shown to be involved inpopulation regulation during quorumsensing in bacteria [5], it has not beengenerally recognised as an importantcomponent of population sensing inunicellular eukaryotes.

Recent work has shown that cell–cellcommunication within oceanicphytoplankton populations may besignificantly more complex thanpreviously thought. Moreover, theinvolvement of PCD in regulatingpopulation growth appears to operateduring both abiotic and bioticinteractions. For example, terminationof bloom growth of the coccolithophoreEmiliania huxleyi has been associatedwith viral infection [6,7]. Indeed, it hasbeen proposed that viral infectionmay be a key agent in the terminationof phytoplankton blooms moregenerally [8]. Significantly, Bidle et al.[9] have shown that viral infection ofE. huxleyi is associated withupregulation of metacaspase proteinexpression and increased caspase-likeactivity, a key component of PCDin cells.

When diatom populations aresubjected to grazing by copepodsthey may release aldehydes that canreduce the reproductive capacity ofthe copepod population, potentiallyproviding an anti-grazing strategy(Figure 1) [10]. Increased aldehyeproduction by diatoms has also beenshown to occur in response to nutrientlimitation [11]. Two recent keypublications shed additional light onthese intriguing interactions. First,Vardi et al. [12] showed that thepennate diatom Phaeodactylumtricornutum and the centric diatomThalasiosira pseudonana respondedto challenge with the aldehyde (2E,4E/Z)-decadienal (DD) by producingnitric oxide (NO). Phaeodactylumcells expressing the luminescentaequorin calcium indicator alsodisplayed calcium signals inresponse to DD challenge. At highconcentrations, DD led to cell death,whereas pre-treatment with low DDconcentrations could prime cells to bemore resistant to DD. The downstreamresponses of this signalling pathwayhave now been dissected in moredetail in a second study from thesame group and reveal that the lethaleffects of higher DD concentrationsare indeed due to PCD. In this issue

Nutrientlimitation

Light stress

Grazing

Calcium signaling

DD

DD

DD

Increased ptNOA1

Current Biology

NO production

Caspase activation

Programmed cell death

Figure 1. Chemical signalling and programmed cell death in diatoms.

Abiotic (nutrient limitation, light stress) and biotic (grazing) factors can lead to intracellularcalcium signals [18] and the formation of aldehydes (DD) that may both suppress grazingactivity and trigger a PCD pathway in neighbouring cells involving calcium signalling and nitricoxide (NO) production. A key role for nitric-oxide-associated protein (NOA) in linking the earlysignals to those mediating cell death has recently been shown.

Multisensory Integration: A LateBloomer

Under many circumstances, human adults integrate information from differentsensory modalities, such as vision and hearing, in a statistically optimalfashion. New results suggest that optimal multisensory integration onlydevelops in middle childhood.

Marc O. Ernst

Some environmental properties, suchas the positions, sizes, and orientations

of objects, can be estimated viamultiple senses, including vision andtouch. Multisensory signals cantherefore carry redundant information.

DispatchR519

of Current Biology, Vardi et al. [13]now show that expression of thegene PtNOA1 (nitric oxide-associatedprotein), which encodes a GTP-bindingprotein belonging to the highlyconserved YqeH subfamily, isincreased in response to challengewith DD. By genetically manipulatingPhaeodactylum cells to overexpressPtNOA1, Vardi et al. [13] have revealeda number of critical downstreamresponses in what appears to bea complex signalling pathway.Interestingly, PtNOA1 was shownto localise to the chloroplast.Overexpression of PtNOA1 led toincreased production of NO andsuppression of a plastid-localisedsuperoxide dismutase (MnSOD) thathad been shown to be an essentialcomponent of oxidative-stressresponses in diatoms [14]. Otherphysiological effects of PtNOA1overexpression included reducedphotosynthetic efficiency, reducedgrowth, increased metacaspaseexpression and increased caspaseactivity. Adhesion of Phaeodactylumto its substrate was also compromisedby the overexpression of PtNOA1.The authors propose that PtNOA1 actsas a switch in regulating thresholdresponses to environmental stress.While it is not yet known whetherPtNOA1 is essential in this signallingpathway, since the gene has yet tobe experimentally knocked down,this work indicates that PtNOA1 hasa significant role in integratingexternal chemical cues with growthresponses and, ultimately, cell death.

While there are many examples ofcell–cell communication in the marineenvironment, including quorumsensing by marine bacteria [15,16],the role of PtNOA1 reveals one of thefirst examples of cell-death signalspotentially acting both to reducegrazing pressure directly and to inducecell death in the grazed population.This new study by Vardi et al. [13]provides compelling evidence thatchemical signals released by diatomsin a population may be perceived byothers, potentially amplifying andspreading a message throughoutthe population. It is becoming morewidely appreciated that PCD may havebenefits for population growth andturnover of unicellular organisms (forexample, see [3]). While the detailedecological implications of PCD inphytoplankton populations are stillfar from clear, it is very likely that

the occurrence of PCD confersa selective advantage. In some casesthis advantage may be obvious. Forexample, in certain dinoflagellates,activation of PCD pathways inresponse to oxidative stress underlimited CO2 availability has beenshown to lead to spore formation and,potentially, dispersal of the populationto a more favourable growthenvironment [17]. In diatoms, there isno evidence that PCD gives rise to anysuch dispersal mechanisms; however,there appears to be significantselective advantages associated withthe removal of damaged orcompromised cells from the populationby allowing resource recycling toactively growing cells [3]. It is alsopossible that this may be part ofa complex mechanism that reduces thenumbers of cells available in regions ofhigh grazer density, providinga secondary control ofgrazer population growth.

References1. Ianora, A., Boersma, M., Casotti, R.,

Fontana, A., Harder, J., Hoffman, F., Pavia, H.,Potin, P., Poulet, S.A., and Toth, G. (2006).New trends in marine chemical ecology.Estuaries Coasts 29, 531–551.

2. Berges, J.A., and Falkowski, P.G. (1998).Physiological stress and cell death in marinephytoplankton: induction of proteases inresponse to nitrogen or light limitation.Limnol. Oceanogr. 43, 129–135.

3. Bidle, K.D., and Falkowski, P.G. (2004). Celldeath in planktonic, photosyntheticmicroorganisms. Nat. Rev.Microbiol. 8, 643–655.

4. Berman-Frank, I., Bidle, K.D., Haramaty, L., andFalkowski, P.G. (2004). The demise of themarine cyanobacterium, Trichodesmium spp.,via and autocatalysed cell death pathway.Limnol. Oceanogr. 49, 997–1005.

5. Kolodkin-Gal, I., Hazan, R., Gaathon, A.,Carmeli, S., and Engelberg-Kulka, H. (2007).A linear pentapeptide is a quorum-sensingfactor required for mazEF-mediated cell deathin Escherichia coli. Science 318, 652–654.

6. Schroeder, D.C., Oke, J., Malin, G., andWilson, W.H. (2002). Coccolithovirus(Phycodnaviridiae): Characterisation of a newlarge dsDNA algal virus that infects Emilianiahuxleyi. Arch. Virol. 147, 1685–1698.

7. Jacquet, S., Heldal, M., Iglesias-Rodriquez, D.,Larsen, A., Wilson, W.H., and Bratbak, G.(2002). Flow cytometric analysis of an Emilianiahuxleyi bloom terminated by viral infectionAquat. Microb. Ecol. 27, 111–124.

8. Suttle, C.A. (1994). The significance of virusesto mortality in aquatic microbial communities.Microb. Ecol. 28, 237–243.

9. Bidle,K.D., Haramaty, L.,Barcelos,E.,Ramos,J.,and Falkowski, P. (2007). Viral activation andrecruitment of metacaspases in the unicellularcoccolithophore, Emiliania huxleyi. Proc. Natl.Acad. Sci. USA 104, 6049–6054.

10. Ianora, A., Miralto, A., Poulet, S.A.,Carotenuto, Y., Buttino, I., Romano, G.,Casotti, R., Pohnert, G., Wichard, T., Colocci-D’Amato, L., et al. (2004). Aldehyde suppressionof copepodrecruitment in bloomsof aubiquitousplanktonic diatom. Nature 429, 403–407.

11. Ribalet, F., Wichard, T., Pohnert, G., Ianora, A.,Miralto, A., and Casotti, R. (2007). Age andnutrient limitation enhance polyunsaturatedaldehyde production in marine diatoms.Phytochemistry 68, 2059–2067.

12. Vardi, A., Formiggini, F., Casotti, R.,De Martino, A., Ribalet, F., Miralto, A., andBowler, C. (2006). A stress surveillancesystem based on calcium and nitric oxidein marine diatoms. PLoS Biol. 4, e60.

13. Vardi, A., Bidle, K., Kwityn, C., Thompson, S.M.,Callow, J.A., Callow, M.E., Falkowski, P., andBowler, C. (2008). A diatom gene regulatingnitric-oxide signaling and susceptibility todiatom-derivedaldehydes.Curr.Biol. 18, 895–899.

14. Wolfe-Simon, F., Starovoytov, V.,Reinfelder, J.R., Schofield, O., andFalkowski, P.G. (2006). Localization and role ofmanganese superoxide dismutase in a marinediatom. Plant Physiol. 142, 1701–1709.

15. Joint, I., Downie, A., and Williams, P. (2007).Bacterial conversations: talking listening andevesdropping. Philos. Trans. Roy. Soc. 362,1115–1117.

16. Joint, I.R., Tait, K., Callow, M.E., Callow, J.A.,Milton, D., Williams, P., and Camara, M. (2002).Cell-to-cell communication across the prokaryote-eukaryote boundary. Science 298, 1207.

17. Vardi, A., Berman-Frank, I., Rozenberg, T.,Hadas, O., Kaplan, A., and Levine, A. (1999).Programmed cell death of the dinoflagellatePeridinium gatunense is mediated by CO2limitation and oxidative stress. Curr. Biol. 9,1061–1064.

18. Falciatore, A., Formiggini, F., and Bowler, C.(2001). Perception of environmental signalsby a marine diatom. Science 288, 2363–2366.

Marine Biological Association of the UK,The Laboratory, Citadel Hill,Plymouth PL1 2PB, UK.E-mail: cbr@MBA.ac.uk

DOI: 10.1016/j.cub.2008.05.003