Algal Symbioses

Angela E Douglas, University of York, York, UK

Algae (including cyanobacteria) enter into symbioses with protists, animals, fungi and plants. They contribute to the nutrition of their partners through photosynthetic carbon fixation and, for cyanobacteria, nitrogen fixation.

Secondary article
Article Contents
. Introduction . Algal Animal Symbioses . Algal Higher Plant Symbioses . Algal Algal Symbioses . Algal Fungal Symbioses

Introduction
The symbiotic algae are members of the two major groups of photosynthetic microorganisms with oxygenic photosynthesis: the eukaryotic algae and cyanobacteria. Their associations with animals, plants, fungi and protists are founded on the algaes possession of metabolic capabilities absent from their partner. Chief among these capabilities is photosynthetic carbon xation, of value to nonphotosynthetic partners under illuminated conditions with low combined carbon availability. The capacity of some symbiotic cyanobacteria to x nitrogen contributes to the nitrogen nutrition of certain plants and fungi. (see Algal photosynthesis.) (see Cyanobacteria.) (see Photosynthesis: ecology.) (see Photosynthetic carbon metabolism.) (see Nitrogen xation.) The symbiotic algae are taxonomically diverse and have evolved from nonsymbiotic algae many times. Table 1 shows the principal taxa. The eukaryotic algal symbionts are dominated by members of two phyla: the Chlorophyta, which are very common symbiotic algae in association with both lichenized fungi (e.g Trebouxia) and freshwater animals and protists (Chlorella); and the Dinophyta, which include the symbiotic algae (e.g. Symbiodinium) in many benthic marine animals and protists. Many of the symbiotic cyanobacteria are members of the Nostocales, lamentous forms with a morphologically distinct cell type, the heterocyst, capable of nitrogen xation. Most symbiotic lamentous cyanobacteria have been assigned to the genus Nostoc, although the taxonomy of the symbiotic cyanobacteria has long been recognized as confused. Unicellular symbiotic cyanobacteria in protists include the cyanelles, forms that have characteristics reminiscent of organelles. (see Algae: phylogeny and evolution.) (see Chlorophyta (green plants).) (see Protist systematics.) Some algal symbioses are of very considerable ecological and economic importance. For example, the symbiosis between dinoagellate algae and corals underpins all shallow-water coral reefs, global biodiversity hotspots worth an estimated $375 billion per annum; and the symbiosis between lichenized fungi and various algae and cyanobacteria are the most important primary producers in habitats covering an estimated 8% of the land surface. The association between Azolla and cyanobacteria is of agricultural importance as a manure in southeast Asia. (see Dinoagellates.) (see Lichens.) (see Microbial symbioses.)

Algal Animal Symbioses

The most widespread symbiotic taxa in animals are the dinoagellate Symbiodinium in the marine environment and the chlorophyte Chlorella in freshwaters (Table 1). Other symbiotic algae/cyanobacteria with a more restricted distribution include: the green cyanobacteria

Table 1 A survey of the common symbiotic algae and cyanobacteria Alga Eukaryotic algae Chlorophyta Chlorophyceae Trebouxiophyceae Dinophyta Gymnodiniales Cyanobacteria Nostocales Representative algal genera Symbiotic partners

Chlorella Trebouxia Symbiodinium

Freshwater ciliates, sponges, hydras Lichenized fungi Benthic marine animals, including many Cnidaria (corals, etc.) and tridacnid clams Some lichenized fungi; higher plants (bryophytes, cycads, Azolla spp., Gunnera spp.)

Nostoc, Calothrix

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Algal Symbioses

Prochloron in ascidians; cyanobacteria, especially Aphanocapsa and Phormidium species in about 38 genera of marine sponges; and various taxa in marine atworms, e.g. the diatom Licmophora sp. in Convoluta convoluta and the prasinophyte Tetraselmis convolutae in C. roscoensis. (see Dinoagellates.) (see Cyanobacteria.) The partners of algae or cyanobacteria include various protist groups, e.g. ciliates, foraminiferans, radiolarians, and the simplest animals, the sponges (Porifera), Cnidaria (corals, sea anemones, hydras, etc.) and the atworms (Turbellaria). These animals comprise thin sheets of tissue of high surface area/volume, well suited to light capture for photosynthesis. Symbiotic algae are also borne by certain bivalve molluscs, including the tridacnid clams. In most associations, the symbiotic algae are restricted to certain anatomical regions of the animal. In Cnidaria, they are almost invariably intracellular, located in the endodermal (inner) of the two body layers; in atworms, they form a coherent layer, probably within animal cells, just internal to the body musculature; in sponges, they are in the mesohyl; and in tridacnid clams they are extracellular, located in the multiply branching diverticula of the gut underlying the mantle tissue. In most associations, the algae account for just 110% of the total biomass of the association. Exceptionally, the cyanobacteria in some sponges represent up to 50% of the total biomass. (see Porifera (sponges).) (see Cnidaria (coelenterates).) (see Marine communities.) (see Mollusca (molluscs).) Ultrastructural studies consistently show the intracellular algae in Cnidaria to be located in symbiosomes, bounded by an animal membrane (Figure 1). This membrane bears adenosine triphosphatase (ATPase) activity, probably linked to the active translocation of nutrients or ions, and carbonic anhydrase activity, which promotes the availability of carbon dioxide to the enclosed algal cell. There is evidence that the pH in the symbiosomal space is not acidic and, for marine systems, the Na 1 concentration is lower than in the surrounding sea water, but conditions within the symbiosomal membrane (osmotic pressure, ionic composition etc.) are, in other respects, unknown (Allemand et al., 1998). The algal cells gain access to all their elemental requirements through the symbiosomal membrane, and the net transfer of sulfur and phosphorus from the animal to algae has been demonstrated in several associations. However, the algae are most unlikely to have free access to the animals nutrient pools and the algae in some marine Cnidaria are nitrogen- or phosphorus-limited. (see ATPases: ion-motive.)

Figure 1 Photosynthetic algae, Symbiodinium sp., in sea anemone Anemonia viridis. The algal cells are coccoid, with permanently condensed chromosomes in the nucleus (n) and a peripheral plastid (p). Bar, 3 Tm. Transmission electron micrographs: A. E. Douglas.

Functions of symbiotic algae

Extensive radiotracer studies with H14CO3 have revealed that the symbiotic algae photosynthesize at high rates, and that much of the recently xed carbon is released from the algal cells to the animal tissues in the form of one or a few
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compounds, usually of low molecular weight. For the Chlorella in freshwater animals, the released compound is the disaccharide sugar, maltose. The marine dinoagellate symbiont, Symbiodinium, may variously release glycerol, glucose, organic acids and amino acids. By the radiotracer technique, 3050% of xed carbon is recovered from the animal tissues, but this may systematically underestimate the true extent of release because much of the xed carbon transferred to the animal may be respired and rexed by the algal cells. Consistent with this interpretation, detailed carbon and energy budget analyses indicate that the algae in several coral species release more than 90% of their photosynthetically xed carbon to the animal tissues, and that this is sucient to meet the total respiratory demands of the animal, at least in well-illuminated shallow waters. (see Algal photosynthesis.) (see Algal carbon dioxide concentrating mechanisms.) (see Algal metabolism.) (see Ecology of invertebrate nutrition.) The algae have also been implicated in the nitrogen nutrition of animals. The most striking indication of the impact of algae on the nitrogen metabolism of animal hosts is that animals experimentally deprived of their algae excrete nitrogenous waste compounds, e.g. ammonia, uric acid, at much higher rates than animals containing algae. Although many aspects of the nitrogen relations of these symbioses need to be resolved, the consensus view is that the algae recycle the animal nitrogenous waste compounds in the synthesis of organic nitrogenous compounds, e.g. amino acids, that are translocated back to the animal tissues. Nitrogen recycling may contribute to the persis-

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Algal Symbioses

tence of these symbioses in low-nutrient waters, especially on coral reefs. (see Nitrogen xation.) (see Invertebrate metabolism.) The cyanobacteria in various sponges may provide products of both carbon and nitrogen xation to the sponge, although this has not been investigated in detail. They have also been implicated in the production of bioactive compounds that protect the sponge from predation or overgrowth by other organisms. One of the best characterized examples is cyanobacterium Oscillatoria spongeliae in the IndoPacic sponge Dysidea herbacea, which synthesizes polybrominated biphenyl ethers, compounds with potent antibiotic properties accounting for up to 12% of the sponge dry weight (Faulkner et al., 1994). However, many of the secondary compounds in sponges are synthesized by the animal tissues, e.g. the cytotoxic alkaloids in Haliclona symbiosis with the dinoagellate Symbiodinium are of sponge origin. (see Antibiotics.) (see Porifera (sponges).)

Synthesis and specificity

The source of algae/cyanobacteria in symbiosis varies with the taxon of their partners. Among protists, the symbionts are generally transmitted vertically at asexual reproduction but not in sexually produced gametes (although many protist symbioses remain to be investigated). In animals, the cyanobacteria of marine sponges are transmitted vertically; the algae in atworms and molluscs (e.g. tridacnid clams) are acquired from the environment; and both modes of acquisition are displayed in Cnidariaalga symbioses. Because the ospring of many animals are algafree and acquire their complement of algae from the environment, free-living populations are presumed to exist. However, symbiotic algae and cyanobacteria of animals and protists have rarely been identied in isolation from their animal partners. (see Reproduction and life cycles in invertebrates.) The specicity of symbioses between algae and animals varies between animal species, but it is commonplace for dierent animal species in one habitat to bear phylogenetically distinct algae. In some animal species, the identity of the symbiotic algae varies with environmental circumstance. For example, the intertidal sea anemone Anthopleura elegantissima associates with both green algae and dinoagellates, and, although both types may coexist in some animals, the green alga is most frequently present in animals on the lower shore and at high latitudes, while the dinoagellate tends to occur on the upper shore and at low latitudes. Two broad processes are likely to contribute to the variation: specic signal exchange between the animal and algal cells, resulting in the discrimination between algae that do, and do not, form the symbiosis; and variation in the habitat requirements between dierent algae, e.g. with respect to temperature and irradiance,

shaping their availability to infect animals and capacity to promote animal growth. However, the molecular basis of the putative signalling between algae and animals remains obscure and there is only fragmentary information on the habitat requirements of dierent algae. (see Dinoagellates.) (see Green algae.) Many symbioses between algae and animals involve a single algal genotype. Processes that restrict the diversity of algae have been investigated experimentally. For example, in freshwater hydras, an established symbiosis with one Chlorella strain is not vulnerable to invasion by a dierent Chlorella strain (i.e. resident wins); and although juvenile animals of the atworm Convoluta roscoensis can be infected by multiple Tetraselmis species, all but one is lost from the animal tissues, such that the mature symbiosis is unialgal. Although the underlying mechanisms are unknown, the resultant low diversity of symbiotic algae in individual animals is widely interpreted to be advantageous to the animal by minimizing competitive interactions among the algae. There are, however, exceptions. Phylogenetically distant algae coexist in many foraminiferans and in some animals (e.g. Anthopleura, considered above) and multiple genotypes of Symbiodinium occur frequently in certain coral species, e.g. Montastrea annularis (Rowan and Knowlton, 1995). (see Biogeography of freshwater algae.) (see Competition.)

Persistence of the symbioses

In all symbioses with animals maintained under uniform conditions in the laboratory, the algae proliferate in apparent harmony with the growing animal tissues, such that the density of algal cells is remarkably uniform. Longterm studies of algal symbioses in the eld have, to date, been conducted only on the coral symbioses and these indicate considerable seasonal and interannual uctuations in algal density that can be attributed, at least in part, to changes in nutrient availability, temperature, irradiance, etc. (Fagoonee et al., 1999). In some symbioses, the gross rate of increase of the algal population is greater than that of the surrounding animal tissues, and overgrowth of the animal by the algal cells is circumvented by the lysis or elimination of excess algal cells. This mode of regulation of the algal population has been particularly well documented for Symbiodinium in sea anemones and corals, which regularly expel coherent pellets of algal cells and animal material via the mouth. The expelled Symbiodinium cells may be disrupted or viable, varying between animal species. The possible signicance of animal-mediated digestion of algal cells as a supplementary source of nutrients for the animal, and of the viable expelled cells in sustaining free-living populations of symbiotic algae, have been discussed widely but not resolved. (see Ecology of invertebrate nutrition.)
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Algal Symbioses

Many animals expel much or all of their algal population when exposed to extremes of, for example, temperature or salinity. This massive loss of algae is aptly described as bleaching because the animals lacking the algae (and their photosynthetic pigments) are white. The cellular processes underlying bleaching are not understood. For Symbiodinium, damage to photosystem II of the algal photosynthetic centres is involved (Warner et al., 1999), and expulsion by the animal has been suggested to reect the collapse of nutritional interactions with the algae. Over the last 20 years, the frequency and severity of bleaching of corals and allied animals has increased dramatically, probably in response to increased sea temperature, often accompanied by increased irradiance, associated with global climate change. Often, the algal population recovers in the weeks to months following bleaching, but the growth, sexual reproduction and resistance to mechanical damage and disease of the coral is depressed; and some bleaching episodes have resulted in mass coral mortality. The long-term implications on coral reefs of repeated bleaching is generally accepted to be detrimental and, in some scenarios, bleaching is considered as a major factor to contribute to the predicted collapse of many of the worlds coral reefs in the coming decades. (see Photosystem II.) (see Algal pigments.) (see Algal ecology.)

Algal Higher Plant Symbioses

Cyanobacteria enter into symbioses with representatives of all the major groups of higher plants, but these associations involve very few plant genera (Table 1): angiosperms of the genus Gunnera, pteridophytes of the genus Azolla (waterferns), many cycad species, and a few bryophytes (e.g. the liverworts Blasia and Calvicularia, the hornworts Anthoceros and Phaeoceros, and some species of the moss Sphagnum). The symbiotic cyanobacteria in these plants are all Nostocales and most of the well-studied forms are of the genus Nostoc, although Calothrix has been identied in the cycad Encephalartos and the hornwort Phaeoceros. The cyanobacteria in Azolla species, although traditionally described as Anabaena azollae, is almost certainly of the genus Nostoc. (see Cyanobacteria.) (see Angiosperms.) (see Pteridophytes (ferns).) (see Bryophytes (hornworts).) The location of the cyanobacteria varies between the dierent plant groups (Figure 2). In Gunnera, the cyanobacteria are intracellular, in mucilage glands at the base of leaves; in Azolla, the cyanobacteria are in cavities of the dorsal lobe of bilobed leaves that emerge from the freeoating, prostrate stems; in cycads, they are in intercellular cortical spaces of specialized apogeotropic roots; in hornworts and liverworts, they are in small cavities opening to the ventral surface of the gametophytic thallus; and in Sphagnum mosses they are in hyaline cells.
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Figure 2 Nitrogen-fixing cyanobacteria in plants. (a) Filaments of the cyanobacteria in a cavity of the water fern Azolla. Bar, 10 Tm. (b) Intracellular cells of the cyanobacteria in the glad cells of Gunner magallenica. Bar, 5 Tm. Scanning electron micrographs of R. Honegger, reproduced from Douglas (1994).

Functions of symbiotic algae

In the symbiosis, the frequency of heterocysts, the nitrogen-xing cells, in the cyanobacterial laments is high, e.g. 2030% in the mature cavities of Azolla, 3050%

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in the hornwort Anthoceros. These data suggest that the symbiotic cyanobacteria may x nitrogen at high rates, as has been conrmed for associations involving representatives of all four plant groups. In the well-studied Anthoceros and Azolla symbiosis, the net transfer of xed nitrogen to the plant has been demonstrated, and ammonia has been identied as the translocated compound. Sustained ammonia release is linked to the low activity of a key enzyme in ammonia assimilation by cyanobacteria, glutamine synthetase. In the cyanobacteria of Azolla, glutamine synthetase synthesis is repressed; in the Anthoceros cyanobacteria, the enzyme is inactivated. The capacity of the symbiotic cyanobacteria for photosynthetic carbon xation is very low, and in the Gunnera symbiosis it is undetectable. The cyanobacteria are dependent on the plant for combined carbon. In Anthoceros, the cyanobacteria probably acquire photosynthetically xed sucrose from the plant. (see Nitrogen xation.) (see Photosynthesis and respiration in cyanobacteria.) (see Mutualistic symbioses.) (see Bryophytes (liverworts).)

higher plants and cyanobacteria (see above), in that the principal role of the cyanobacteria is nitrogen xation. One association of this class has been studied: between the marine diatoms of several genera (e.g. Hemiaulus, Rhizosolenia) and heterocystous cyanobacteria, Richelia intracellularis (Janson et al., 1999). This association can attain high populations in the tropical and subtropical oceans, where it may contribute up to 15% of the total nitrogen xed (Carpenter et al., 1999). (see Diatoms.)

Algal Fungal Symbioses

The dominant symbioses of algae and cyanobacteria with fungi are the lichens. In the lichen literature, the symbiotic algae or cyanobacteria in lichens are usually known as photobionts and their fungal partner as the mycobiont. Lichens are classied in terms of the fungal partner, and almost all lichen species are ascomycetes. An estimated 85% of lichen species bear eukaryotic algae, with 10% containing cyanobacteria and up to 5% containing both algae and cyanobacteria. The taxonomy of the photobionts is poorly studied but the available information suggests that Trebouxia is widely distributed, found in about half of all lichen species. Other eukaryotic photobionts include some members of 3040 genera of chlorophyte algae (e.g. Coccomyxa, Pleurococcum, Myrmecia and Trentepohlia), the xanthophyte (e.g. Heterococcus) and the phaeophyte (e.g. Petroderma). The dominant cyanobacterial photobionts are lamentous forms of the genera Nostoc and Scytonema, but representatives of other groups have been described, e.g. Gloeocapsa (Chroococcales) and Stigonema, Hyphomorpha and Fischerella (Stigonematales). The lamentous cyanobacteria in some lichens are contorted and have the form of packets of cells. (see Lichens.) (see Fungi: ecological importance and impact on humans.) In all lichens, the photobiont cells are extracellular. More than half of all lichens are small and inconspicuous, and comprise an amorphous aggregate of fungal hyphae and photobiont cells. The interactions between the photobiont and fungus in these microlichens are poorly understood. Most research concerns the macrolichens, which have a well-dened growth form (foliose, fruticose, etc.) and are usually stratied into distinct layers, including a symbiont layer in which the photobionts are positioned in an ordered array (Figure 3a). In the symbiosis between Parmelia species and Trebouxia, the processes generating the regular spacing between algal cells have been established. The cell wall of each algal cell is contacted by a single fungal projection (Figure 3b). As the Trebouxia cell divides, the fungal projection branches, makes contact with each algal daughter cell, and lengthens, so separating out the algal cells. (see Algal cell walls.) (see Hyphae.) (see Algal reproduction.) (see Ascomycota.)
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Synthesis and specificity

The symbioses are not highly specic (Nilsson et al., 2000). Nostoc isolated from Gunnera, Azolla and Anthoceros readily form symbioses with cyanobacteria-free plants of all three groups in laboratory conditions (cycads have not been studied in this respect); and in one study of eld populations of hornwort Phaeoceros, 30 genotypes of Nostoc and one Calothrix were isolated, all of which could form a symbiosis with a dierent plant, the liverwort Anthoceros, in the laboratory (West and Adams, 1997). (see Bryophytes (liverworts).) In all the symbioses except Azolla, the cyanobacteria are acquired from the environment. Short, motile laments of Nostoc (called hormogonia) infect preformed cavities of bryophytes and leaf glands of Gunnera and enter the cycad roots via cracks in the root dermis. A chemotactic response of the hormogonia to components of plant mucilage may promote synthesis of the symbiosis. The symbiosis in Azolla is unusual in that the cyanobacteria are transmitted vertically, by insertion under the cap of each sporocarp, and the symbiosis is tightly integrated into the development of the plant. Specically, cyanobacteria are maintained at the shoot apex and, as the cavity is formed in each developing leaf, it acquires an inoculum of cyanobacteria from the apex. As a result, each Azolla plant is rarely, if ever, infected by free-living cyanobacteria under natural circumstances.

Algal Algal Symbioses

Symbioses between eukaryotic algae and cyanobacteria are functionally analogous to the relationship between

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Algal Symbioses

The morphologically complex macrolichen thallus is generated only in symbiosis with algae or cyanobacteria. When grown in culture, the fungi are morphologically unremarkable. Furthermore, the identity of the photobiont can determine lichen morphology. For example, some lichenizing fungi may associate with both cyanobacteria and eukaryotic algae simultaneously and, in these circumstances, the alga is located in most of the thallus and the cyanobacteria is restricted to specialized, gall-like structures called cephalodia. The lichen Sticta lix can also associate with algae and cyanobacteria; it has foliose morphology with algae, and fruticose morphology with cyanobacteria. It is generally accepted that the photobionts make no morphogenetic contribution to lichen morphology, but trigger preexisting developmental pathways in the fungus. There have been many attempts to reconstitute the lichen thallus from the separate partners (Stocker-Wo rgo tter, 1995). The methodology is technically demanding, involving coculturing the fungus and photobionts for many months under low-nutrient conditions, often with regular wetting/drying cycles. Of the many lichen species tested, very few species (e.g. Cladonia cristatella, Xanthoria parietina) have been synthesized successfully. Distinct from the lichen symbiosis is the unusual association between Nostoc and the fungus Geosiphon pyriforme. In this system, the cyanobacterial laments are intracellular within bladders.

Functions of symbiotic algae

The photobionts in lichens are photosynthetically active. The photosynthetic rate per unit chlorophyll is comparable to that of related nonsymbiotic algae or cyanobacteria, but depends critically on the water content of the lichen thallus. Lichens are poikilohydric, i.e. their water content varies with environmental conditions, from 25% to 150300% dry weight. The maximum photosynthetic rate usually occurs at 5080% saturation of the thallus (i.e. when the thallus is damp rather than wet). Reduced photosynthetic rates at high water content can be attributed to increased carbon dioxide diusion resistance as lichen air spaces are lled with water. At low water content, the fungus and photobiont cells lose physiological activity. In general, the eukaryotic algae maintain photosynthetic activity at lower water levels than cyanobacteria and this restricts most lichens with cyanobacteria to habitats of relatively high water availability. (see Algal photosynthesis.) (see Photosynthesis and respiration in cyanobacteria.) (see Chlorophylls.) The photobionts release up to 80% of their photosynthetically xed carbon to the fungus. In 14C radiotracer studies, substantial amounts of xed carbon are recovered from the fungal layer. Photosynthetic carbon is released in the form of one or a few compounds. The cyanobacteria release glucose and the eukaryotic algae release polyhydric

Figure 3 The stratified lichen thallus of Parmelia borreri. (a) Vertical section through thallus, showing the algal symbionts (s) sandwiched between two symbiont-free layers, the dorsal cortex (c) and ventral medulla (m). Bar, 10 Tm. (b) Morphology of the contact between the fungus and algal symbiont, Trebouxia. Each symbiont cell is in contact with a single fungal projection (arrow). Bar, 1 Tm. Scanning electron micrographs of R. Honegger, reproduced from Douglas (1994).

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alcohols, also called polyols (e.g. ribitol from Trebouxia and Coccomyxa, sorbitol from Stichococcus, erythritol from Trentepohlia). The mechanisms underlying photosynthate translocation are not understood, but passive uxes of solutes when membrane permeability barriers are impaired during periods of desiccation and rehydration may be important. The fungal partner in lichens metabolizes the carbon derived from the photobiont to polyols, especially mannitol, which can account for up to 10% of thallus dry weight. The polyols are not storage compounds but stress metabolites of crucial importance to the lichen tolerance of variable water content. When a lichen thallus of low water content is wetted (for example by a drop of rain), substantial amounts of solutes are lost from the thallus over a period of 12 min and the lichen respiration rate is greatly elevated for up to 2 h. The photobiontderived polyol pool provides all the carbon lost in these processes, with apparently minimal perturbation of other fungal metabolite pools. The polyols are also important to the physiological integrity of lichen thalli of very low water content because their hydroxyl groups replace bound water associated with proteins and other macromolecules, preventing denaturation. (see Photosynthetic carbon metabolism.) (see Plant response to water-decit stress.) The cyanobacteria in lichens x nitrogen, in addition to carbon. Where they are the sole photobiont, their nitrogen xation rates are broadly equivalent to those in nonsymbiotic cyanobacteria and the frequency of heterocysts (the cells responsible for nitrogen xation) is generally 4 8%. Where eukaryotic algae are present and the cyanobacteria are restricted to cephalodia, nitrogen xation rates are elevated by up to an order of magnitude and heterocyst frequencies are 3040%. Much of the xed nitrogen is transferred to the fungus (c.5060% from cyanobacteria as sole symbionts; 4 90% for cyanobacteria in cephalodia), exclusively in the form of ammonia. Paralleling the condition of nitrogen-xing cyanobacteria in higher plants, the cyanobacteria in lichens have very low activity of the enzyme in ammonia assimilation, glutamine synthetase, and the ammonia is believed to diuse freely out of the cyanobacterial cells. It is taken up rapidly by the fungus and assimilated into amino acids via glutamate dehydrogenase. (see Nitrogen xation.) The cyanobacteria Nostoc in Geosiphon pyriforme x both carbon by photosynthesis and atmospheric nitrogen, and the transfer of photosynthetic carbon to the fungus has been demonstrated (Kluge et al., 1991). Many lichens contain secondary compounds, often known as lichen substances. Lichenization is important for the synthesis of these compounds, which are not produced by the isolated fungus in culture. The involvement of the photobionts in the synthesis of lichen substances is, however, indirect (perhaps through the supply of photosynthetic carbon), and there are no indications that the photobionts synthesize these secondary compounds.

The advantage to the algae of the symbiosis with lichenized fungi has been disputed for many years. There is now clear evidence that the fungus provides no waterstress protection to the photobiont (Honegger, 1991), and the photobiont cells have very restricted or no access to fungal nutrients. In strictly physiological terms, the photobionts can be considered as parasitized by the fungus.

Synthesis and specificity

Some photobiont lineages may persist indenitely in the lichen symbiosis without a free-living stage. Many individual lichen thalli can persist for centuries, and asexual propagules of lichenized fungi generally bear photobiont cells from the parental thallus. In addition, in certain instances, the photobiont can be transferred between dierent fungal partners without exiting from the symbiotic condition. Specically, the germinating spores of some fungal species can infect established lichen thalli of dierent fungal species, kill the fungus and take over the symbiotic algae (e.g. Xanthoria parietina can usurp Physcia tenella, and Diploschistes muscorum can usurp Cladonia pocillum). However, most of the lichenized fungi that reproduce by spores depend on contact with appropriate photobionts in the free-living condition to reestablish the symbiosis, even though the photobionts of lichens are generally rare or unknown apart from the lichen symbiosis. Many lichens are moderately specic, i.e. several closely related species of algae or cyanobacteria can form a symbiosis with one fungal species; however, virtually no information is available on the signal exchange between the photobionts and fungi that leads to the development of the fully dierentiated lichen thallus, either from an asexual propagule or from initial contact between a germinating fungal spore and free-living photobiont cells. The development of the symbiosis can be divided into three broad stages: (1) nonspecic contact; (2) prethallus stage, comprising an amorphous undierentiated structure reminiscent of the morphology of microlichens; and (3) the mature stratied thallus. Analyses of lichen synthesis with eukaryotic algae in the laboratory indicate that lichenizing fungi contact and form a prethallus with a range of algae, but the transition to the stratied thallus is much more specic. For example, X. parietina develops into a stratied, foliose lichen in association with certain Trebouxia species, but fails to dierentiate beyond a prethallus with other Trebouxia and Pleurococcus species. A protein that specically binds to the surface of compatible algae has been isolated from the cell wall surface of X. parietina hyphae, but its signicance in vivo has not been studied.

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Algal Symbioses

References
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Stocker-Wo rgo tter E (1995) Experimental cultivation of lichens and lichen symbionts. Canadian Journal of Botany 73: S579589. Warner ME, Fitt WK and Schmidt GW (1999) Damage to photosystem II in symbiotic dinoagellates: a determinant of coral bleaching. Proceedings of the National Academy of Sciences of the USA 96: 8007 8012. West NJ and Adams DG (1997) Phenotypic and genotypic comparison of symbiotic and free-living cyanobacteria from a single eld site. Applied and Environmental Microbiology 63: 44794484.

Further Reading
Ahmadjian V (1993) The Lichen Symbiosis. New York: Wiley. Bergman B, Matveyev A and Rasmussen U (1996) Chemical signalling in cyanobacterial-plant symbioses. Trends in Plant Sciences 1: 191197. Douglas AE (1995) Ecology of symbiotic micro-organisms. Advances in Ecological Research 26: 69103. Muscatine L (1990) The role of symbiotic algae in carbon and energy ux in reef corals. In: Dubinsky Z (ed.) Ecosystems of the World: Coral Reefs, pp. 7587. Amsterdam: Elsevier. Nash TH (1995) Lichen Biology. Cambridge: Cambridge University Press. Peters GA (1991) Azolla and other plantcyanobacterial symbioses: aspects of form and function. Plant and Soil 137: 2536. Trench RK (1998) Diversity of symbiotic dinoagellates and the evolution of microalgalinvertebrate symbioses. In: Lessios HA and Macintyre IG (eds) Proceedings of the 8th International Coral Reef Symposium, pp. 12751286. Balboa, Republic of Panama: Smithsonian Tropical Research Institute.

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