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.

Abstract

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 evolutionary success of these symbioses is evident from the wide range of animal groups that have established associations with chemosynthetic bacteria; at least seven animal phyla are known to host these symbionts. The diversity of the bacterial symbionts is equally high, and phylogenetic analyses have shown that these associations have evolved on multiple occasions by convergent evolution. This Review focuses on the diversity of chemosynthetic symbionts and their hosts, and examines the traits that have resulted in their evolutionary success.

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Figure 1: Chemosynthetic symbioses in different marine habitats.
Figure 2: Symbioses found at deep-sea hydrothermal vents.
Figure 3: Symbioses found both at deep-sea hydrothermal vents and cold seeps.
Figure 4: Symbioses in bivalves from shallow-water habitats.
Figure 5: Symbioses in worms and protists from shallow-water habitats.
Figure 6: Phylogenetic diversity of gammaproteobacterial, chemosynthetic symbionts based on their 16S ribosomal RNA gene sequences.

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Acknowledgements

This work was supported by the Max Planck Society, the German Research Foundation (DFG) Cluster of Excellence at MARUM Bremen, and the DFG-Priority Program 1144: From Mantle to Ocean: Energy-, Material- and Life-cycles at Spreading Axes (contribution number 28). We are grateful to the Census of Marine Life working group ChEss for its support of research on the biogeography of chemosynthetic ecosystems. We particularly thank the members of the Symbiosis Group of the Max Planck Institute Bremen for their enthusiasm about and discussions of chemosynthetic symbioses. We also thank the anonymous reviewers for helpful suggestions that improved this review. Much of the early literature on chemosynthetic symbioses is not cited here owing to space limitations.

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Glossary

Chemolithoautotrophic

Chemolithoautotrophic organisms use a chemical compound as an energy source, an inorganic compound, such as sulphide, as an electron donor and an inorganic carbon source (usually carbon dioxide) to synthesize organic carbon.

Phototrophic

Phototrophic organisms, such as plants, use light to gain energy.

Heterotrophic

Heterotrophic organisms, such as humans, use an organic source of carbon.

Chemoautotrophic

The term chemoautotrophic is often used as a synonym for chemolithoautotrophic. However, some chemoautotrophs use organic compounds as electron donors; these organisms are called chemoorganoautotrophs.

Chemosynthetic

Describes two types of organisms: chemolithoautotrophs (for example, sulphur oxidizers) and methane oxidizers. These organisms convert one or more carbon molecules (usually carbon dioxide or methane) into organic matter using the oxidation of inorganic compounds (for example, sulphide) or methane as a source of energy. Both symbiotic and free-living chemosynthetic microorganisms are primary producers; they form the basis of the food chain at vents and seeps.

Thiotrophic

An organism that uses reduced sulphur compounds, such as sulphide, as electron donors is called a thiotroph or sulphur oxidizer.

Meiofauna

Small free-living invertebrates that live in marine and fresh-water sediments. Meiofauna do not constitute a defined taxonomic rank but rather are a group of benthic animals that are defined by their size (in general, these organisms can pass through a 1 mm sieve, but are retained on a 0.45 μm sieve).

Epibiont

A symbiont that lives on the surface of its host.

Endobiont

A symbiont that lives inside its host.

Methanotrophic

An organism that uses methane as an energy and carbon source is called a methanotroph or methane oxidizer.

Syntrophy

Strictly defined, syntrophy describes a nutritional relationship between two organisms that combine their metabolic capabilities to use a substrate that neither could use alone. In this Review, we use syntrophy loosely to describe the beneficial exchange of products between two or more organisms.

Population bottleneck

An evolutionary event in which the size of a population is greatly reduced.

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Dubilier, N., Bergin, C. & Lott, C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6, 725–740 (2008). https://doi.org/10.1038/nrmicro1992

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