The Influence of Symbiont Diversity on the Functional Biology of a Model Sea Anemone

Cnidarian–dinoflagellate symbioses, particularly those between anthozoans and dinoflagellates of the genus Symbiodinium (commonly referred to as zooxanthellae) are widespread in the marine environment. They are responsible for the formation of coral reefs and are thus of great ecological importance. In recent years there has been an increase in the frequency and severity of episodes of coral bleaching resulting in degradation and mortality of coral reefs on a global scale. In order to gain a deeper understanding of how corals can adapt to changing environmental conditions, the effect that symbiont type has on the persistence and physiology of an association needs to be ascertained. The aim of this research was to determine how different symbiont types affect the nutritional biology and intracellular physiology of the symbiosis when in association with the sea anemone Aiptasia pulchella. The specific objectives of the study were to; (1) determine whether different symbiont types are equally as adept at supporting the energetic demands of the same host; (2) determine if internal pH (pHi) is a reflection of symbiont type and whether the optimal pH for photosynthesis coincides with the host cell pHi; and (3) test the influence of Symbiodinium type on host tissue glycerol and glucose pools. In order to answer these questions, aposymbiotic (i.e. symbiont-free) sea anemones were infected with different Symbiodinium types and the relationship between symbiont type, photosynthetic performance and autotrophic potential was tested. A range of ‘normal’ and novel cnidarian–dinoflagellate symbioses was also used to measure host cell pHi and to determine the optimal pHi of isolated intact symbiosomes (i.e. the vacuoles that house the symbionts), as well as to compare the amounts of free glycerol and glucose (metabolites) present in the host tissues. Different host-symbiont combinations were found to have different photosynthetic and respiratory attributes. Earlier onset of full autotrophy (i.e. when all metabolic carbon demands of the symbiosis were met by photosynthesis) and higher CZAR values (i.e. the contribution of zooxanthellae to animal respiration) were demonstrated by symbioses hosting Symbiodinium B1 both from the original (homologous) and different (heterologous) host. The study showed that Symbiodinium types differ in their pH optima and that the optimal pHi for photosynthesis does not always match the actual measured pHi. Symbiont type was also shown to have an effect on host tissue glycerol and glucose pools, with the associations harbouring the homologous Symbiodinium B1 attaining the highest concentrations of both metabolites. Findings from this study suggest that corals may be able to maintain an association with a range of Symbiodinium types, and hence potentially switch as a consequence of bleaching. The new symbiont type may not be as nutritionally advantageous as the original type however, which could have implications for the growth and survivorship of the coral, unless it is able to supplement its carbon demands heterotrophically. The rapid proliferation of some of the heterologous Symbiodinium types (e.g. Symbiodinium E2) inside the host indicates that, after bleaching, there is potential for fast symbiont establishment. The reduced carbon contribution of these heterologous symbionts may not be a major concern should the coral be able to reinstate the more nutritionally advantageous symbiont as the dominant type during bleaching recovery. Finally, the rapid proliferation demonstrated by the heterologous Symbiodinium types and the associated metabolic cost to the host, could be an indication of the opportunistic nature of some of these types and may indicate a shift towards parasitism. It is imperative to extend this type of work to corals in the field to determine how these associations behave in nature. Also, in order to get a clearer picture of the diversity in symbiosis physiology, a wider range of Symbiodinium types needs to be investigated.