Symbiotic diversity in marine animals: the art of harnessing chemosynthesis

Key Points Chemosynthetic symbioses between bacteria and marine invertebrates were discovered 30 years ago at hydrothermal vents on the Galapagos Rift. Remarkably, it took the discovery of these symbioses in the deep sea for scientists to realize that chemosynthetic symbioses occur worldwide in a wide range of habitats, including cold seeps, whale and wood falls, shallow-water coastal sediments and continental margins. The most well known habitats for chemosynthetic symbioses are those in the deep sea. Deep-sea hydrothermal vents were the first habitats to be discovered in which chemosynthetic rather than photosynthetic primary production fuels large animal communities that are considered to belong to some of the most productive on the Earth. When organic matter falls to the deep-sea floor in the form of whale carcasses or sunken wood (named whale and wood falls), it supports chemosynthetic communities for limited periods of time. Only at vents and seeps do these associations dominate the biomass and form large standing crops. At whale and wood falls, chemosynthetic symbioses form only a small part of the animal community. A remarkable number of animals have established symbioses with chemosynthetic symbionts. The morphological diversity of chemosynthetic associations is also high, showing the adaptive flexibility of both the animals and the microorganisms in these associations. In addition to morphological diversity, the behavioural and physiological strategies used by animals to supply their symbionts with both reductants and oxidants vary markedly, even within closely related host groups. Until recently, the diversity of chemosynthetic symbionts was considerably underestimated. Progress in the molecular techniques that have been used to detect microbial diversity has led to the realization that more than two endosymbionts can co-occur in both deep-sea and shallow-water hosts. Just as molecular analyses have led to the discovery of unrecognized phylogenetic diversity, genomic and proteomic analyses are beginning to reveal the metabolic diversity of chemosynthetic symbionts.