Journal of Experimental Botany, Page 1 of 12

doi:10.1093/jxb/erm328

SPECIAL ISSUE REVIEW PAPER

Photosynthetic symbioses in animals

A.A. Venn1,*, J.E. Loram1,* and A.E. Douglas2,†

1 Bermuda Institute of Ocean Sciences, Ferry Reach, St Georges GE01, Bermuda2 Department of Biology, University of York, PO Box 373, York YO10 5YW, UK

Received 1 May 2007; Revised 24 October 2007; Accepted 29 October 2007

Abstract

Animals acquire photosynthetically-fixed carbon by

forming symbioses with algae and cyanobacteria.

These associations are widespread in the phyla Por-

ifera (sponges) and Cnidaria (corals, sea anemones

etc.) but otherwise uncommon or absent from animal

phyla. It is suggested that one factor contributing to

the distribution of animal symbioses is the morpholog-

ically-simple body plan of the Porifera and Cnidaria

with a large surface area:volume relationship well-

suited to light capture by symbiotic algae in their

tissues. Photosynthetic products are released from

living symbiont cells to the animal host at substantial

rates. Research with algal cells freshly isolated from

the symbioses suggests that low molecular weight

compounds (e.g. maltose, glycerol) are the major

release products but further research is required to

assess the relevance of these results to the algae in

the intact symbiosis. Photosynthesis also poses risks

for the animal because environmental perturbations,

especially elevated temperature or irradiance, can lead

to the production of reactive oxygen species, damage

to membranes and proteins, and ‘bleaching’, including

breakdown of the symbiosis. The contribution of non-

photochemical quenching and membrane lipid compo-

sition of the algae to bleaching susceptibility is

assessed. More generally, the development of geno-

mic techniques to help understand the processes

underlying the function and breakdown of function in

photosynthetic symbioses is advocated.

Key words: Bleaching, Chlorella, Cnidaria, coral, metabolite

profiling, nutrient release, photosynthesis, Symbiodinium,

symbiosis, symbiotic algae.

Introduction

Oxygenic photosynthesis has apparently evolved justonce, in the lineage that gave rise to all extant cyanobac-teria (Cavalier-Smith, 2006). This metabolic capabilityhas, however, been acquired on multiple occasions byeukaryotes through symbiosis either with cyanobacteria orwith their unicellular eukaryotic derivatives genericallytermed ‘algae’. Overall, 27 (49%) of the 55 eukaryoticgroups identified by Baldauf (2003) have representativeswhich possess photosynthetic symbionts or their deriva-tives, the plastids. These include the three major groups ofmulticellular eukaryotes: the plants, which are derivativesof the most ancient symbiosis between eukaryotes andcyanobacteria; the fungi, many of which are lichenizedwith algae or cyanobacteria; and the animals. We, theauthors, and probably many readers were taught thatanimals do not photosynthesize. This statement is true inthe sense that the lineage giving rise to animals did notpossess plastids, but false in the wider sense: manyanimals photosynthesize through symbiosis with algae orcyanobacteria.

This article on ‘photosynthesis in animals’ focuses onthe central role of photosynthesis in symbioses betweenalgae and animals, by considering three topics: theimportance of light capture as a factor limiting thedistribution of the symbioses in the animal kingdom;photosynthate transfer to the animal host, especially theunderlying mechanisms and significance to the animalhost; and risks to the symbiosis posed by photosyntheticreactions in the plastids of symbiotic algae. Two issues arebeyond the scope of this article. These are the transientanimal associations with photosynthetically-active chloro-plasts obtained from algae consumed by the animal, andthe significance of symbiotic algae to the animal hostbeyond the nutritional role of photosynthesis. In particu-lar, some algal symbionts contribute to the nitrogen

* These authors contributed equally to this publication.y To whom correspondence should be addressed. E-mail: aed2@york.ac.uk

ª The Author [2008]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.For Permissions, please e-mail: journals.permissions@oxfordjournals.org

Journal of Experimental Botany Advance Access published February 10, 2008

relations of their hosts by acting as a sink for animalmetabolic waste, especially ammonia. Furthermore, thealgae may recycle nitrogen, i.e. assimilate ammonia intocompounds valuable to the host, such as essential aminoacids, which are released to the host. Early approaches toexplore nitrogen recycling were experimentally flawed(see the discussion in Wang and Douglas, 1998), butrecent approaches exploiting stable isotope techniques areyielding firm indications of nitrogen recycling in somesymbioses (Tanaka et al., 2006).

Distribution of photosynthetic symbiosesin animals

Most animals with photosynthetic symbioses are membersof two phyla, the Porifera (the sponges) and Cnidaria(including the hydroids, corals, sea anemones, andjellyfish) (Table 1). The dominant algal symbionts inthese animals are freshwater chlorophytes of the genusChlorella found, for example, in Spongilla sponges andfreshwater hydras; dinoflagellates of the genus Symbiodi-nium in benthic marine hosts, including virtually all reef-building corals in the photic zone; and cyanobacteria inmany marine sponges. These two animal phyla aremorphologically simple and traditionally considered asthe basal animal groups.

Animal body plan may contribute to the distribution ofphotosynthetic symbioses in animals. The body plans ofboth Porifera and Cnidaria inherently have a large surfacearea:volume relationship promoting the capture of light tomeet the demands of the bulk tissue for photosyntheti-cally-derived carbon. In particular, the Cnidaria arediploblast animals, comprising just two sheets of cells(the outer epidermis and inner gastrodermis) and can bemoulded, through natural selection, into a variety ofshapes; in his book on sea anemones, Malcolm Shick(1991) aptly terms these animals ‘origami animals’. Allother animals have the triploblast body plan, i.e. witha third body layer derived from the embryonic mesoderm.

The triploblast body plan is ‘solid’, generally of lowsurface area per unit volume, and with limited capacity forextensive evaginations suitable for the absorption of light.Consistent with this distinction, photosynthetic symbiosesin triploblastic animals is largely restricted to flatworms(turbellarian platyhelminths) constrained, despite theirpossession of mesoderm, to a large surface area:volumerelationship by their lack of circulatory system (Table 1).

Photosynthetic symbioses do, however, occur in a fewmolluscs, which are large and morphologically complexanimals; and molluscan hosts display considerable mor-phological adaptation for the symbiotic habit, an in-dication that the basic body form is not well-suited tophotosynthesis. The tridacnid molluscs (family Tridac-nidae: giant clams) are particularly informative. This groupcomprises five species, including Tridacnis gigas of up to180 kg weight, and they all bear photosynthetic algalsymbionts of the dinoflagellate genus Symbiodinium. Thetridacnids differ from other bivalve molluscs in thatthe body is rotated through 180� relative to the hinge, andthe siphonal tissue is hypertrophied, such that the ‘gape’of the shell reveals the siphonal tissue and mantle of theanimal, and not the foot as in other bivalves. Accompany-ing this radical re-organization of the body plan toaccommodate photosynthesis, the digestive tract is trans-formed into multiple dichotomously branching diverticulabearing Symbiodinium cells and projecting towards thelight—like branches of a tree (Norton et al., 1992). Theseremarkable morphological adaptations are a consequenceof the poor compatibility of photosynthesis and themassive body form characteristic of most triploblasticanimals.

These considerations should not, however, be inter-preted to mean that photosynthesis poses no morpholog-ical conflict for the diploblast Cnidaria. Themorphological conflict for Cnidaria is particularly evidentin relation to the animals’ tentacles, especially of seaanemones and their allies. Most Cnidaria with symbioticalgae are also carnivores, and in most species prey items

Table 1. Survey of symbioses between animals and photosynthetic symbionts

Hosts Symbionts References

Porifera Cyanobacteria in many marine sponges, Lee et al., 2001Symbiodinium in clionid (boring) marine sponges,Chlorella in freshwater sponges, e.g. Spongilla

Cnidaria Symbiodinium in benthic marine corals, sea anemones etc. Stat et al., 2006Scripsiella spp. in pelagic taxa, e.g. Velella Banaszak et al., 1993Chlorella in freshwater hydra

Platyhelminthes Various in marine turbellarians, e.g. Tetraselmis (prasinophyte) Parke and Manton, 1967in Symsagittifera (¼Convoluta) roscoffensis; Apelt and Ax, 1969Licmophora (diatom) in Convoluta convoluta Douglas, 1987Chlorella in freshwater turbellarians, e.g. Dalyella spp

Mollusca Dinoflagellates, usually Symbiodinium in marine gastropods and Belda-Baillie et al., 2002bivalves, including tridacnid clams; Chlorella in few freshwaterclams, e.g. Anodonta

Ascidia Cyanobacteria, usually Prochloron in various ascidians Lewin and Chang, 1989

2 of 12 Venn et al.

are trapped by nematocysts on the animals’ tentacles.(Nematocysts are organelles which subdue prey by theirtoxic barbs and adhesive secretions prior to ingestion.)Food capture is promoted by the possession of relativelyfew, long, mobile tentacles with a high density ofnematocysts; and photosynthesis is promoted by largenumbers of short tentacles with high densities of symbi-otic algal cells. Most of the Cnidaria which obtainnutrition by a combination of feeding and photosynthesisdisplay morphological ‘compromise’ in relation to theirtentacles. The several exceptions are informative.

The remarkable sea anemone Lebrunia danae hasdimorphic tentacles. One form of its tentacles lackssymbiotic algae and is long and slender, suited forfeeding; and the other form is short but branched anddensely colonized by Symbiodinium (Fig. 1A). Interfer-ence between the two tentacle types is avoided in theliving animal by specific extension of the feeding tentaclesat night, when food is available in the water column, andphotosynthetic tentacles by day, for light capture. Themorphology of the two tentacles is so different that

L. danae was originally classified as a member of twodifferent genera.

Other sea anemones have resolved the conflict by theevolution of novel structures for either feeding orphotosynthesis. In Bunodeopsis species, the tentacles arepredominantly feeding structures and the Symbiodiniumalgae are concentrated in vesicles on the body column(Fig. 1B). By day, the vesicles inflate by the accumulationof sea water, so maximizing the surface area for lightcapture, with the tentacles retracted; and the reverseoccurs at night (Day, 1994). Discosoma species adopta different morphological strategy (Fig. 1C). Thesecoralliomorph cnidarians have small, ‘stubby’ tentaclesalmost entirely devoid of nematocysts, and food capture ismediated by the lateral expansion of the oral disc (theupper surface of the body column bearing the mouth andtentacles) to form a muscular ‘oral veil’. When prey makecontact with the oral disc, the oral veil extends rapidly up-and-over the prey, which is essential ‘bagged’ beforetransfer whole via the mouth to the gut (Elliott and Cook,1989).

Fig. 1. Morphological adaptations for light capture in sea anemones with photosynthetic symbionts. Scale bars¼2.5 cm. (a) Dimorphic tentacles ofLebrunia danae (i) photosynthetic tentacles and (ii) colourless feeding tentacles emerging in response to a prey item. (b) Vesicles on the body wall ofBunodeopsis antilliensis bearing symbiotic algal cells: at night, when feeding tentacles are extended; and by day when the feeding tentacles areretracted and the vesicles expanded. (Photographs of R Day.) (c) Tentacles on the oral disc of Discosoma sanctithome (i), and capture of small fishprey by extension of the oral veil (2–4, see text for details). (Photographs of B Watson.)

Photosynthesis in animals 3 of 12

These various morphological adaptations are indicativeof the selective advantage of symbiosis with algae fortheir animal hosts. A key basis of this selective advantageis host access to alga-derived photosynthetic carbon,which is considered in the next section.

Host access to photosynthetic carbon fixed bysymbiotic algae

Algal cells in symbiosis with animals are photosyntheti-cally competent, fixing carbon dioxide and releasingoxygen at rates (per cell or per unit chlorophyll) at leastcomparable to algal cells in culture. In most animal hosts,the algal cells are intracellular, bounded by an animalmembrane, known as the symbiosomal membrane. Asa result, they obtain the carbon dioxide and water for thephotosynthetic reaction and all substrates required forsynthesis of cellular constituents, including the photosyn-thetic apparatus, from the host cell. Delivery of substrateshas involved biochemical and cellular adaptation by theanimal. In particular, marine cnidarians bearing Symbiodi-nium, first, maintain high activity of carbonic anhydraseand, second, have specific transporters for the deliveryof bicarbonate ions to the cells bearing the symbioticalgae. These traits provide a partial pressure of CO2 inthe immediate surroundings of the symbiont cells that ishigh enough to support photosynthetic carbon fixation(Allemand et al., 1998).

Radiotracer experiments with 14C-bicarbonate demon-strate that the algae release up to 50% of photosyntheti-cally-fixed carbon to the animal host; and these valuesmay be underestimates because of incomplete penetrationof 14C-radioisotope in short-term experiments, and re-spiratory loss of radioactivity from the animal as CO2

which is refixed by the algal cells. Photosynthate release isbiotrophic (i.e. from living cells) and apparently selective,with the dominant photosynthetic products of the algalcells apparently ‘protected’ from release.

Much research has focused on the identity of thecompounds translocated to the animal tissues; thesecompounds are known as ‘mobile’ compounds (Table 2).There has been a strong expectation that the mobilecompounds are dominated by one (or a few) compoundsof low molecular weight, by analogy with the release oftriose phosphate from chloroplasts and single polyolsfrom the algal symbionts in lichens. Early research on thesymbiotic Chlorella in freshwater hydra appeared toconfirm this expectation. When the Chlorella cells areisolated from hydra and incubated immediately in simplebuffer of pH 4–5 under illumination, they release largeamounts of the disaccharide maltose. Metabolic analysesrevealed that the maltose is synthesized within 1 min ofcarbon fixation and derived from a small metabolic poolwith high turnover (Cernichiari et al., 1969). It wasconcluded, entirely plausibly, that maltose is the mobile

compound of symbiotic Chlorella. Consistent with thisinterpretation, non-symbiotic Chlorella do not releasephotosynthate in response to low pH. Doubt over therelevance of this research with freshly-isolated Chlorellahas been cast subsequently, with the demonstration thatthe pH in the immediate environment of Chlorella in thesymbiosomal space in the symbiosis is >5.5, and wouldnot be expected to induce substantial maltose release(Rands et al., 1992).

Studies seeking to identify the processes mediatingphotosynthate release and the identity of the mobilecompounds in symbioses with Symbiodinium has alsofocused on algal cells freshly-isolated from the symbiosis.Photosynthate release from isolated Symbiodinium cells isnot triggered by manipulation of pH of the medium, but itis induced by the addition of ‘a drop of’ homogenate ofthe host tissues (Trench, 1971). The active component inthe host homogenate has variously been identified asproteinaceous (Sutton and Hoegh-Guldberg, 1990) andamino acids, including high concentrations of proteinamino acids (Gates et al., 1995) and micro-molar concen-trations of the non-protein amino acid, taurine (Wang andDouglas, 1997), but its identity remains elusive. Its modeof action involves modification of algal metabolism (Grantet al., 2006), and it can be mimicked by clotrimazole(1-a-2 chlorotrityl imidazole) (Ritchie et al., 1997),raising the possibility that the host factor is an antagonistof calmodulin and may modulate Ca2+-calmodulin-mediated signalling in either the animal or algal cell.Symbiodinium cells incubated with host homogenate

release various low molecular weight compounds derivedfrom photosynthesis, including glycerol, organic acids,glucose, and amino acids, the composition and diversityof released compounds varying among different symbio-ses and studies (Trench, 1979). The factors contributing tothis variation may include homogenate composition,genotype, and metabolic condition of Symbiodinium andthe protocol used for separation and identification ofreleased compounds. These uncertainties notwithstanding,these data suggest that the mobile compounds of Symbio-dinium are not derived directly from a single metabolicpool in the alga. In other words, photosynthate releasefrom Symbiodinium is likely to be more complex meta-bolically than from the plastids of plants and symbioticChlorella.

Just as with the Chlorella system, there is doubt overthe relevance of the traits of isolated Symbiodinium to theintact symbiosis. Perhaps the most telling study wasconducted by Ishikura et al. (1999) on Symbiodinium inthe giant clam Tridacna crocea. Unlike the symbioses incorals and other Cnidaria, Symbiodinium is extracellularin tridacnids, making direct analysis of the photosyntheticcompounds released from the algae in symbiosis techni-cally feasible. Ishikura et al. (1999) demonstrated that thedominant compound released by the algae in T. crocea is

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Table 2. Photosynthetic products released from photosynthetic symbionts in animals

Host Symbiont Experimental Technique Mobile Compounds References

Porifera Marine Cyanobacteria 14C tracer experiments: isolated algae Glycerol and a small organic Wilkinson, 1979Fresh water Chlorella sp. 14C tracer experiments: isolated algae

with comparison to metabolism of 14C-glucose in vivo

Glucose Wilkinson, 1980

14C tracer experiments: isolated algae Glucose Fischer et al., 1989Cridaria Coral Symbiodinium 14C tracer experiments: freshly isolated

algae with or without hosthomogenate.

glycerol, sugars, organic acids andamino acids

Muscatine, 1967; Sutton and HoeghGuldberg, 1990; Gates et al., 1995,Grant et al., 1997 Hinde, 1988, Lewisand Smith, 1971

Measurement of respiratory quotients Glycerol in shallow colonies (< 5m)and lipid in deeper colonies (30 m)

Gattuso and Jaubert, 1990

Identification of dinoflagellate (algal)-specific compounds in animal tissue

Polyunsaturated fatty acids Papina et al., 2003

14C tracer experiments with NaH14CO2

and 14C acetate: intact symbiosesLipid Patton et al., 1983

14C tracer experiements with 14C-acetate : isolated algae and intactsymbiosis.

Lipid Patton et al., 1977

14C tracer experiments with 14C-glucose: intact symbiosis.

Lipid Oku et al., 2003

Anemones Symbiodinium 14C tracer experiments: isolated algae dGlycerol, glucose, alanine and organicacids

Trench, 1971 Lewis and Smith, 1971

14C tracer experiments with partialuncoupling of photosyntheis andrespiration: intact symbiosis andisolated algae

Glycerol Battey and Patton, 1987

Metabolite profiling: intact symbiosis Glucose, succinate/fumarate Whitehead and Douglas, 2003Identification of symbiosis-specificcompounds in animal tissue

Triglyceride Harland et al., 1991

14C tracer studies with 14C-acetate:intact symbiosis and isolated algae

Lipid Blanquet et al., 1979

Metabolism of NaH14CO3, 14C-acetateand 14C-glucose: intact symbiosis

Glycerol and lipid. Battay and Patton, 1984

Metabolism of 14C-aspartate and14C-glutamate in aposymbiotic andsymbiotic anemones

Essential amino acids Wang and Douglas, 1999

Zoanthids Symbiodinium 14C tracer experiments: isolated algae Organic acids, amino acids and sugars von Holt and Holt, 1968b Lewis andSmith, 1971

Gorgonians, Jelly-fishand Hydrozoans

Symbiodinium 14C tracer experiments: isolated algaeusing inhibition technique

Glycerol, glucose, alanine Lewis and Smith, 1971

Fresh water Hydra Chilorella 14C radiotracer studies: isolated algae Maltose Mews, 1980Platyhelminthes Tetraselmis 14C radiotracer studies: intact

symbiosisAmino acids Particularly alanine Muscatine et al., 1974 Botyle and

Smith, 1975Mollusca Tridacnid clams Symbiodinium 14C tracer studies: isolated algae Glycerol Muscatine, 1967 Streamer et al., 1988;

Rees et al., 199314C tracer studies: intact symbiosis Glucose Ishikura et al., 1999Carbon isotopic [13C] analysis ofanimal and algal tissue

16:0 and 16:1 fatty acids Johnston et al., 1995

Sacoglossan seaslugs

Chloroplasts fromfood alga

14C tracer studies on isolatedchlorolasts/homogenized tissue

Glucose, alamine, glycolic acid Gallop, 1974; Trench et al., 1973

14C tracer studies impact symbiosis Glucose, galactose, mannose, alanine Trench et al., 1974Chordata Ascidians Prochloron 14C tracer on isolated algae Glycolate Fisher and Trench, 1980

Photosynthesis

inanim

als

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glucose in the symbiosis but glycerol in isolated algalpreparations. The implication that photosynthate releaseinduced by host homogenate may be mechanisticallydifferent from that in symbiosis, and consequentlyartefactual, has led to a renewed interest in the study ofphotosynthate release in the intact symbiosis.

One approach with considerable potential to study theidentity of the mobile compounds of symbiotic algae ofanimals is metabolite profiling (Whitehead and Douglas,2003). The rationale of this method is that, over a periodof one-to-several min , the animal host metabolizes themobile compounds to a ‘signature’ panel of products thatis also produced when the animal takes up the samecompounds from the exogenous medium. In other words,exogenous compounds that yield the ‘signature panel’ ofanimal products are likely to be the mobile compounds.Using this approach, candidate mobile compounds forSymbiodinium in the sea anemone Anemonia viridis havebeen identified as glucose and the dicarboxylic organicacids succinate and fumarate. As analytical methods forthe identification and quantification of metabolites im-prove, the utility of this method to pinpoint candidatemobile compounds for further investigation will increase.

An important message to emerge from these consid-erations concerns the experimental approach to studyphotosynthate release from symbiotic algae. Our under-standing of photosynthate release comes principally fromresearch on isolated algae, but insufficient attention hasbeen given to the relevance of the findings to the traits ofthe algae in symbiosis. Although there is no basis to‘write off’ all research with isolated algae as artefact,future research on isolated algal preparations should seekstrategies to check the compatibility of results with theinteractions in the intact symbiosis.

In comparison to the uncertainty over the mechanismsunderlying photosynthate release from symbiotic algaeand the identity of the mobile compounds, there iswidespread acceptance that photosynthetic products de-rived from the symbiotic algae are important to the animalhost [although even this point is also contested, forexample by Goreau (2006)]. Circumstantial evidenceincludes the apparent absence of alga-free individuals ofmost animal species capable of forming the symbiosis innatural habitats, and the depressed growth rates of mostsymbioses incubated in continuous darkness. Classicalbudget analyses particularly of Muscatine et al. (1984)and Davies (1984) indicate that photosynthetic carbonderived from Symbiodinium is sufficient to meet much orall the total carbon requirement for basal respiration inseveral coral species. In some coral species, much of thephotosynthetic carbon is allocated to mucus, which isproduced in copious amounts and is important in feedingand protection from mechanical damage and pathogens. Asignificant proportion of the photosynthate received by theanimal is not, however, dissipated rapidly (Rinkevich,

1989; Tanaka et al., 2006), and this includes photosyn-thetically-derived carbon in the animal lipid pools (Gro-tolli et al., 2004), which are crucial for gametogenesis andsexual reproduction in corals and other Cnidaria (Araiet al., 1993).

One important generality embedded in these consider-ations is that the algae provide the animal with fixedcarbon. The animals cannot ‘live on’ their algal symbiontsalone. They obtain nitrogen, phosphorus, and otherelements from a combination of dissolved compoundsand, for most taxa, holozoic feeding (Schlicter, 1982;Ferrier, 1991; Grover et al., 2006). In this context, thephotosynthetic algae have been likened to a source of‘junk food’, which meets the immediate energeticdemands and other carbon-based requirements of the host,valuable to the animal in environments where othersources of nutrients are in short supply.

The susceptibility of photosynthetic symbiosesto environmental stress

Photosynthesis brings to animals major risks as well asnutritional benefits. Photosynthesis can be perturbed byupsetting the balance between the rates of light collectionand light use, resulting in the production of reactiveoxygen species (ROS) (Asada, 1996). Left unchecked,ROS are damaging to protein function and membraneintegrity, and pose a serious threat to both the photosyn-thetic symbionts and their animal hosts.

Photosynthetic symbioses in animals respond to certainenvironmental changes by bleaching, literally a loss incolour. Bleaching is caused by the loss of algal pigmentsor elimination of algal cells from the symbiosis (Brown,1997). Most research has concerned bleaching in symbi-oses with Symbiodinium and these symbioses may beparticularly susceptible to environmental perturbation.Because Symbiodinium is the usual symbiont of corals,bleaching is often described as ‘coral bleaching’, but seaanemones, clams and other hosts of Symbiodinium appearto be as susceptible to bleaching as corals. Bleaching canbe triggered by multiple factors (Douglas, 2003; Jones,2004), but most bleaching observed in the field is causedby elevated temperature often acting synergistically withsolar radiation (Fitt et al., 2001; Lesser and Farrell, 2004).The impacts of bleaching include reduced growth andreproduction, increased susceptibility to disease andmechanical damage, and occasionally death of the host(Szmant and Gassman, 1990; Glynn, 1996; Baird andMarshall, 2002). Mass bleaching events in recent yearshas led to the mortality of hosts across entire reefs(Hoegh-Guldberg, 1999).

Photosynthetic corals and other tropical symbioses withSymbiodinium live close to their upper thermal tolerancelimits (Fitt et al., 2001). On the basis of projected

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increases in sea temperature with climate change, massbleaching events and die-offs have been predicted toincrease in frequency and severity over the comingdecades (Hoegh-Guldberg, 1999). Indeed, reef collapsehas been predicted by the 2020s for the Indian Ocean(Sheppard, 2003) and globally by 2050s (Hoegh-Guldberg, 1999). As corals are the foundation to coralreef ecosystems, coral mortality caused by thermalbleaching is a first-order threat to biodiversity in tropicaland subtropical seas.

A large body of evidence now points to the impairmentof algal photosynthesis as a key step in the thermalbleaching of Symbiodinium symbioses. Uncertainty, how-ever, still exists over the sequence of events, and severalsites have been proposed as the position of the initiallesion in algal photosystems (Fig. 2). Iglesias-Prieto et al.(1992) demonstrated a decrease in the efficiency ofPhotosystem II (PSII) when cultured algae were exposedto temperatures of 34–36 �C, leading to the suggestionthat the primary impact of high temperature was to causea malfunction in the light reactions of photosynthesis.Warner et al. (1996) recorded a loss of photosyntheticefficiency in algae in bleached corals subjected to elevatedtemperatures, making a direct link between temperature-dependent impairment of photosynthesis and coral bleach-ing. Furthermore, the degradation of the reaction centreD1 protein co-occurred with temperature-dependent lossof PSII activity (Warner et al., 1999). The D1 protein hasan important structural and functional role in the PSIIreaction centre, binding components for charge separationand electron transport. When PSII is excited there isa probability that damage to the D1 protein will occur.Under normal physiological conditions the rate of photo-damage does not exceed the capacity to repair thedamage, but D1 re-synthesis and replacement maybecome impaired in algae at elevated temperature, leadingto a loss of PSII functional reaction centres (Warner et al.,1999).

An alternative viewpoint is provided by Jones et al.(1998), who argued that damage to PSII was a downstreamimpact of impairment of the Calvin–Benson Cycle.Specifically, these authors suggest that a decrease incarboxylation of ribulose 1,5 bisphosphate (RuBP) byRubisco could lead to reduced rates of consumption ofproducts of the photosynthetic electron transport (ATPand NADPH) restricting the rate of flow in the electrontransport chain (sink-limitation). These events wouldresult in maximal reduction of the plastoquinone pool,causing damage at PSII through a build-up of excessexcitation energy. The net consequence would be theformation of highly reactive triplet states of chlorophyllwhich react with O2 to form singlet oxygen (�O�

2) (Smithet al., 2005). Singlet oxygen is potentially damaging toproteins; it can trigger the degradation of the D1 protein(Asada, 1996) and also react with components in the

light-harvesting antennae leading to bleaching of pigments(Halliwell, 1991).

The Mehler reaction is an alternative sink for electrons.It may help prevent maximal reduction of the PSIIquinone receptors at the point where the rate of light-driven transport exceeds the capacity of the temperature-impaired Calvin cycle (Jones et al., 1998), but at the costof producing ROS (Asada, 1999). The Mehler reactioninvolves reduction of O2 by PSI to produce superoxideradicals that are rapidly converted within the chloroplastto hydrogen peroxide by superoxide dismutase (Fig. 2).Detoxification of hydrogen peroxide to water then occursby ascorbate peroxidase (Fig. 2). Both superoxide dis-mutase and ascorbate peroxidase are present in Symbio-dinium (Matta and Trench, 1991) and under mostconditions the rate of detoxification should exceed the rateof ROS generation. During bleaching, however, ROScould accumulate if the rate of its production exceeds itsremoval (Smith et al., 2005).

Analysis of variable chlorophyll fluorescence kineticsin Symbiodinium by Tchernov et al. (2004) indicates thatelevated temperatures of 32 �C damage thylakoidmembranes causing an increase in the rate of electrontransport on the acceptor side of PSII with a simultaneousdecrease in the maximum quantum yield of photochem-istry in the reaction centre. These changes are diagnosticof energetic uncoupling of electron transport, where thetransmembrane proton gradient, established by thephotochemical reactions in the reaction centres, isdissipated without generating ATP. Thylakoid mem-branes remain capable of splitting water and photosyn-thetically-produced O2 is reduced by the Mehler reactionleading to the accumulation of ROS as described above.Dye tracer experiments conducted by the same authorson algae in culture indicate that the ROS could leak fromalgal cells (Fig. 2).

Whatever the initial site of damage to algal photo-systems, the generation of ROS through temperature-irradiance impairment of photosynthesis presents a sourceof oxidative stress for the algal and animal partners.Oxidative stress can elicit a wide spectrum of cellularresponses (Martindale and Holbrook, 2002), some ofwhich are known to occur in bleaching, for example,exocytosis of algae from host cells (Brown et al., 1995),and lysis of both animal and algal cells by elements ofnecrotic and programmed cell death pathways (Dunnet al., 2002; Franklin et al., 2004). Little is known aboutthe cellular pathways that mediate cellular responses tooxidative stress in animals with photosynthetic symbionts,although these pathways are well described in modelsystems (Martindale and Holbrook, 2002).

Recent research of Perez and Weis (2006) on thesymbiotic anemone Aiptasia pallida provides an indica-tion of the processes involved. Exposure of this symbiosisto heat stress or the photosynthetic inhibitor DCMU

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triggers the production of nitric oxide (NO) in the hostcell, leading to bleaching of the symbiosis. Incubation ofanemones in lipopolysaccharide (LPS) also induces NO ingastrodermal cells of A. pallida to similar levels observedwith elevated temperature and an inhibitor of phtosystem-II. LPS is known to induce an up-regulation of nitricoxide synthase through the nuclear factor jB (NF-jB)-dependent signalling in mammalian systems, and Perezand Weiss (2006) suggest that ROS released from heat-stressed photosystems in the algal cells might induce NOproduction in the host via the similar pathways. Theyspecifically hypothesize that NO converts to cytotoxicperoxynitrite on interaction with superoxide in the hostcell, leading to cell death and bleaching.

A number of mechanisms have evolved in the animalhosts that protect the algal photosystems against elevatedthermal and light stress. For example, corals can retract

soft tissues to reduce light capture (Brown et al., 1994,2002), and symbiotic sea anemones and corals possessa large diversity of SOD isoforms, similar to thosedescribed in terrestrial plants (Richier et al., 2003).Interestingly, corals also possess fluorescent proteins(FPs) which may play a role in ameliorating the impact ofhigh irradiance on algal cells (Salih et al., 2000). Theprotection offered by FPs is reduced at elevated temper-atures however, raising doubts about their photoprotectiverole during thermal bleaching (Dove, 2004).

Algal–animal symbioses vary greatly in their suscepti-bility to bleaching and much of this variation has beenattributed to differences in thermotolerance among algalpartners. Single host species associated with differentalgal genotypes may vary in bleaching susceptibility(Rowan et al., 1997; Perez et al., 2001). Research on themechanistic basis of thermal tolerance in the algal cells

Fig. 2. Three proposed primary impacts of elevated temperature on the photosystems of symbiotic algae in animal hosts, shown as I, II, and III in thefigure. (I) Dysfunction of PSII and degradation of the D1 protein. (II) Energetic uncoupling in the thylakoid membranes. (III) Impairment of theCalvin cycle. During bleaching ROS are generated from O2 via the Mehler reaction and are detoxified by superoxide dismutase (SOD) and ascorbateperoxidase (APX). If the rate of ROS generation exceeds detoxification, then oxidative damage can occur, triggering signalling pathways and cellularresponses that underpin bleaching. Singlet oxygen can be generated at damaged PSII reaction centres and in the photosynthetic antennae causingphotobleaching of chlorophyll and accessory pigments.

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has focused primarily on non-photochemical quenching(NPQ), which can dissipate excess excitation energy intemperature-impaired algal photosystems (Warner et al.,1996). The xanthophyll cycle is a key NPQ mechanismand it has been described in Symbiodinium (Brown et al.,1999; Venn et al., 2006). Conversion of the pigmentsdiadinoxanthin to diatoxanthin (analogous to the xantho-phylls violaxanthin, antheraxanthin, and zeaxanthin interrestrial plants) diverts excess excitation energy awayfrom PSII reaction centres. Although inhibition of xantho-phyll cycling by dithiothreitol (DTT) can lead to increasedoxidative damage in corals (Brown et al., 2002), doubtsover its significance have been raised by the finding thatthe abundance and cycling of xanthophyll pigments is notgreater in bleaching-resistant than bleaching-susceptiblecorals (Venn et al., 2006). Other mechanisms of NPQdescribed in Symbiodinum might contribute to thermaltolerance; they include dissipation of excess excitationenergy as heat within the PSII reaction centres (Gorbunovet al., 2001), and state 1 to state 2 transitions associatedwith phosphorylation and the migration of light- harvest-ing complexes away from PSII (Hill et al., 2005).

Experiments of Tchernov et al. (2004) suggest that lipidsaturation determines the stability of the thylakoidmembranes at elevated temperature. As the same authorsalso found evidence that thermal disruption of thethylakoids is the initial site of damage during bleaching,the membrane lipids of symbiotic algae may determine thebleaching susceptibility of animal–algal symbioses. Cer-tain algal genotypes possess thylakoid membranes witha higher content of the mono-unsaturated fatty acidD9-cis-octadecenoic acid (18:1) relative to the majorpolyunsaturated fatty acid D6,9,12,15-cis-octadecatetrae-noic acid (18:4), affording them stability at elevatedtemperatures.

These findings illustrate a general point: that a variety ofprocesses, from ROS to NO and membrane lipid compo-sition, have all been implicated as determinants ofbleaching and variation in susceptibility to bleaching. Thetask for the future is to establish the relative importance ofthese different processes and how they interact to mediatethe observed bleaching phenomena. This, in turn, willprovide a basis for predicting the scale of future bleachingevents and their impacts on the coral communities, onwhich reef ecosystems depend.

Concluding comments

Photosynthesis in animals has been the focus of sustainedresearch for 40–50 years. Despite this, understanding isvery limited of both how animals exploit this metaboliccapability of their symbiotic algae and how the symbiosisresponds to the risks of ROS and photosystem damage.In comparison to other symbioses, notably the rhizobial–legume associations, the photosynthetic symbioses in

animals have a major handicap of lacking a genetic ‘tool-kit’ that would enable molecular dissection of thesymbiosis based on forward and reverse genetics and geneexpression analysis. Some molecular resources are, how-ever, becoming available, notably EST and BAC libraries,with plans for complete genome sequencing, for the algaland animal partners in Symbiodinium–cnidarian symbio-ses. Furthermore, methods for the genetic transformationof Symbiodinium and RNAi-mediated suppression of hostgene expression have been reported (ten Lohuis andMiller, 1997; Dunn et al., 2007), and these deservesustained investment by the community to promote thedevelopment of robust, general protocols for manipula-tions. These approaches have great potential for identifi-cation of genes underpinning the mechanisms by whichphotosynthesis has been accommodated in animals.

Acknowledgements

The authors acknowledge support from the Khaled Bin SultanLiving Oceans Foundation (AAV), the National Oceanic andAtmospheric Administration (JEL), and The Biotechnology andBiological Sciences Research Council (AED) during the preparationof the review.

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