Multispecies microbial mutualisms on coral reefs: the host as a habitat

Abstract

Reef-building corals associate with a diverse array of eukaryotic and noneukaryotic microbes. Best known are dinoflagellates in the genus Symbiodinium ("zooxanthellae"), which are photosynthetic symbionts found in all reef-building corals. Once considered a single species, they are now recognized as several large, genetically diverse groups that often co-occur within a single host species or colony. Variation among Symbiodinium in host identities, tolerance to stress, and ability to colonize hosts has been documented, but there is little information on the ecology of zooxanthellar free-living stages and how different zooxanthellae perform as partners. Other microbial associates of reef corals are much less well known, but studies indicate that individual coral colonies host diverse assemblages of bacteria, some of which seem to have species-specific associations. This diversity of microbial associates has important evolutionary and ecological implications. Most mutualisms evolve as balanced reciprocations that allow partners to detect cheaters, particularly when partners are potentially diverse and can be transmitted horizontally. Thus, environmental stresses that incapacitate the ability of partners to reciprocate can destabilize associations by eliciting rejection by their hosts. Coral bleaching (the loss of zooxanthellae) and coral diseases, both increasing over the last several decades, may be examples of stress-related mutualistic instability.