The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally

Abstract

The discovery of chemosynthetic ecosystems at deep-sea hydrothermal vents in 1977 changed our view of biology. Chemosynthetic bacteria and archaea form the foundation of vent ecosystems by exploiting the chemical disequilibrium between reducing hydrothermal fluids and oxidizing seawater, harnessing this energy to fix inorganic carbon into biomass. Recent research has uncovered fundamental aspects of these microbial communities, including their relationships with underlying geology and hydrothermal geochemistry, interactions with animals via symbiosis and distribution both locally in various habitats within vent fields and globally across hydrothermal systems in diverse settings. Although ‘black smokers’ and symbioses between microorganisms and macrofauna attract much attention owing to their novelty and the insights they provide into life under extreme conditions, habitats such as regions of diffuse flow, subseafloor aquifers and hydrothermal plumes have important roles in the global cycling of elements through hydrothermal systems. Owing to sharp contrasts in physical and chemical conditions between these various habitats and their dynamic, extreme and geographically isolated nature, hydrothermal vents provide a valuable window into the environmental and ecological forces that shape microbial communities and insights into the limits, origins and evolution of microbial life.

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Fig. 1: Global distribution of hydrothermal-vent systems.
Fig. 2: Microbial habitats at deep-sea hydrothermal vents.
Fig. 3: Generalized characteristics of vents.
Fig. 4: Ecological and biogeochemical interactions at deep-sea hydrothermal vents from a microbial perspective.

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Acknowledgements

The author thanks C. German for input and S. Beaulieu for guidance about the map in figure 1. The author is grateful to the wonderful group of staff, graduate students, postdocs and collaborators who worked on vents with him and helped develop some of the ideas presented here: K. Anantharaman, B. Baker, S. Jain, R. Lesniewski, M. Li, D. Reed, C. Sheik, B. Toner and J. Breier. The Gordon and Betty Moore Foundation Marine Microbiology Initiative supported this research. The preparation of this manuscript was supported by an Alfred P. Sloan Foundation Fellowship in Ocean Sciences.

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Nature Reviews Microbiology thanks K. Takai and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Glossary

Chemosynthesis

The use of chemical energy to fix inorganic carbon into organic carbon for microbial growth.

Microbial mats

Dense, macroscopic communities of microorganisms attached to a solid surface.

Chemolithoautotrophic growth

The growth of bacteria or archaea using an inorganic, chemical source of energy (for example, reduced forms of iron, sulfur, hydrogen and ammonia) to fix inorganic carbon into organic carbon.

Reductive tricarboxylic acid cycle

(rTCA). A metabolic pathway for carbon fixation in which two molecules of carbon dioxide are converted into acetyl coenzyme A; it uses most of the same enzymes as the oxidative tricarboxylic acid cycle but runs it in reverse by using three alternative enzymes: fumarate reductase, 2-oxoglutarate synthase and ATP citrate lyase.

Calvin–Benson–Bassham cycle

A carbon fixation pathway in which carbon dioxide is converted into glyceraldehyde-3-phosphate using the key enzyme Rubisco.

Wood–Ljungdahl pathway

A metabolic pathway for carbon fixation in which two molecules of carbon dioxide are converted into acetyl coenzyme A by the key enzyme carbon monoxide dehydrogenase–acetyl coenzyme A synthase.

Dicarboxylate–4-hydroxybutyrate pathway

A recently described carbon fixation pathway in archaea in which a molecule of bicarbonate (HCO3) is fixed onto acetyl coenzyme A via a combination of enzymes from the reductive tricarboxylic acid cycle and the 4-hydroxybutyrate part of the 3-hydroxypropionate–4-hydroxybutyrate cycle.

Black smokers

Hydrothermal vents that eject plumes of black suspended particles, chiefly iron sulfide minerals.

White smokers

Hydrothermal vents that eject plumes of white suspended mineral particles composed mainly of calcium, barium and silica.

Ultramafic

Relating to igneous rocks that have a very low silica content and very high content of magnesium and iron.

Denitrifying

A type of process in which nitrate is used as an electron acceptor for energy metabolism and is reduced to di-nitrogen gas (denitrification).

Mineral flocs

Flocculent materials sometimes emitted from hydrothermal vents, composed of fine mineral particles and often microbial biomass.

Trophosome

An internal organ in tubeworms used to host chemosynthetic symbiotic bacteria.

Autotrophy

The growth of an organism through the fixation of inorganic carbon into organic carbon.

Heterotrophy

A mode of organism growth in which exogenous organic carbon functions as the source of carbon.

Allopatric speciation

The evolutionary divergence of a population into distinct species due to geographic separation.

Thermohaline conveyor

The global circulation of water in the oceans, driven by density gradients due to differences in the temperature and salinity of water masses.

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Dick, G.J. The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally. Nat Rev Microbiol 17, 271–283 (2019). https://doi.org/10.1038/s41579-019-0160-2

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