Importance of time and place: patterns in abundance of Symbiodinium clades A and B in the tropical sea anemone Condylactis gigantea.

The capacity of some corals and other cnidarians to form symbioses with multiple algae (Symbiodinium) is a candidate route by which these symbioses tolerate variable environmental conditions. On Bermuda, the coral reef dwelling anemone Condylactis gigantea bears Symbiodinium of clades A and B. At thermally variable inshore and nearshore sites, clade A predominates (as sole symbiont or in mixed infection with clade B), whereas animals at offshore sites with more uniform temperatures bear only clade B or mixed infections. Individual animals at one nearshore site monitored over a year by sampling tentacles showed increased prevalence of clade A in March-November, when sea waters were warm (average 26 degrees C), and increased clade B in November-March when cool waters prevailed (average 18.5 degrees C). In laboratory analyses of excised tentacles, the symbiosis with clade B, but not clade A, bleached at elevated temperature (32 degrees C), suggesting that thermal tolerance may contribute to the higher prevalence of clade A at inshore/nearshore sites and in the summer. The temporal changes in the algal complement were not accompanied by bleaching, and Symbiodinium density fluctuated in hosts with stable Symbiodinium composition but not in hosts with variable composition. This suggests that changes in the relative abundance of Symbiodinium clades do not require bleaching and may even protect the symbiosis from large fluctuations in algal density.

Photosynthetic symbioses in animals.

Animals acquire photosynthetically-fixed carbon by forming symbioses with algae and cyanobacteria. These associations are widespread in the phyla Porifera (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 morphologically-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 composition of the algae to bleaching susceptibility is assessed. More generally, the development of genomic techniques to help understand the processes underlying the function and breakdown of function in photosynthetic symbioses is advocated.

Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis.

The giant sea anemone Condylactis gigantea associates with members of two clades of the dinoflagellate alga Symbiodinium, either singly or in mixed infection, as revealed by clade-specific quantitative polymerase chain reaction of large subunit ribosomal DNA. To explore the functional significance of this molecular variation, the fate of photosynthetically fixed carbon was investigated by (14)C radiotracer experiments. Symbioses with algae of clades A and B released ca. 30-40% of fixed carbon to the animal tissues. Incorporation into the lipid fraction and the low molecular weight fraction dominated by amino acids was significantly higher in symbioses with algae of clade A than of clade B, suggesting that the genetically different algae in C. gigantea are not functionally equivalent. Symbioses with mixed infections yielded intermediate values, such that this functional trait of the symbiosis can be predicted from the traits of the contributing algae. Coral and sea anemone symbioses with Symbiodinium break down at elevated temperature, a process known as 'coral bleaching'. The functional response of the C. gigantea symbiosis to heat stress varied between the algae of clades A and B, with particularly depressed incorporation of photosynthetic carbon into lipid of the clade B algae, which are more susceptible to high temperature than the algae of clade A. This study provides a first exploration of how the core symbiotic function of photosynthate transfer to the host varies with the genotype of Symbiodinium, an algal symbiont which underpins corals and, hence, coral reef ecosystems.