Sulfur metabolites in the pelagic ocean

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Abstract

Marine microorganisms play crucial roles in Earth’s element cycles through the production and consumption of organic matter. One of the elements whose fate is governed by microbial activities is sulfur, an essential constituent of biomass and a crucial player in climate processes. With sulfur already being well studied in the ocean in its inorganic forms, organic sulfur compounds are emerging as important chemical links between marine phytoplankton and bacteria. The high concentration of inorganic sulfur in seawater, which can readily be reduced by phytoplankton, provides a freely available source of sulfur for biomolecule synthesis. Mechanisms such as exudation and cell lysis release these phytoplankton-derived sulfur metabolites into seawater, from which they are rapidly assimilated by marine bacteria and archaea. Energy-limited bacteria use scavenged sulfur metabolites as substrates or for the synthesis of vitamins, cofactors, signalling compounds and antibiotics. In this Review, we examine the current knowledge of sulfur metabolites released into and taken up from the marine dissolved organic matter pool by microorganisms, and the ecological links facilitated by their diversity in structures, oxidation states and chemistry.

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Fig. 1: Organic sulfur reservoirs and flux in the pelagic ocean.
Fig. 2: Representative molecular structures and sulfur oxidation states of marine sulfur metabolite classes.
Fig. 3: Biochemical pathways for marine microbial synthesis of sulfur metabolites.
Fig. 4: Biochemical pathways for marine microbial catabolism of sulfur metabolites.
Fig. 5: The ecological network of marine microbial synthesizers and consumers of organic sulfur metabolites.
Fig. 6: Seasonal dynamics of organic sulfur catabolism genes in the oligotrophic ocean.

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Acknowledgements

This work was supported by grants from the Simons Foundation (542391, M.A.M.) and the National Science Foundation (IOS-1656311 and OCE-PRF-1521564). The authors thank S. Sharma, for bioinformatic support, and F. Ferrer-González, B. Nowinski, J. Schreier, W. Schroer, C. Smith and M. Uchimiya, for helpful comments.

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The authors contributed equally to all aspects of the article.

Correspondence to Mary Ann Moran.

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Related links

Bermuda Atlantic Time-Series Study: http://bats.bios.edu

Hawaii Ocean Time-Series Data Organization & Graphical System: http://hahana.soest.hawaii.edu/hot/hot-dogs/index.html

Supplementary information

Glossary

Allelochemicals

Chemicals produced by a living organism that can be beneficial or detrimental to another organism.

Volatile

A molecule that readily vaporizes into air.

Metabolites

Small molecules that are a direct product of metabolism.

Aerosols

Suspensions of solid or liquid particles in gas.

Cloud nucleation

Formation of aerosol particles on which water vapour condenses in the first step of cloud formation.

Osmolytes

Organic molecules used by organisms to maintain cellular water balance.

Assimilation

Process by which organisms transform compounds into organic molecules.

Biosynthesis

The process by which organisms assemble the components of molecules.

Biogeochemical

Relating to the cycling of elements through biological, geological and chemical processes.

Tg

Teragram, 1012 grams.

Stoichiometry

A quantitative measure of the relationship among elements in a chemical compound.

Turnover times

The times required to completely renew the content of reservoirs.

C1 compound

An organic compound that consists of a single carbon atom with attached hydrogen atom(s).

Heterotrophic

Describes an organism that must obtain organic compounds for growth and energy.

Redox state

Ratio of the oxidized and reduced forms of molecules.

Angiosperms

A major evolutionary group of plants that has flowers and produces seeds enclosed within a carpel.

Catabolism

Metabolic breakdown of molecules into smaller forms during the production of energy or for use in other reactions.

Oligotrophic

An environment containing low levels of nutrients.

Entner–Doudoroff

The name of a bacterial pathway that catabolizes glucose to pyruvate.

Mesopelagic

A region of the pelagic ocean about 200–1,000 m below the surface, where light is present but at levels of <1% of incident.

Antimicrobial

A chemical that kills or inhibits the growth of microorganisms.

Deep chlorophyll maximum

A region below the ocean surface where maximum concentrations of chlorophyll are found.

Niche

The set of interactions of a species with the other members of its community and with the abiotic factors of its environment.

Mutualistic

A symbiotic relationship between two organisms that is beneficial to both.

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Moran, M.A., Durham, B.P. Sulfur metabolites in the pelagic ocean. Nat Rev Microbiol 17, 665–678 (2019) doi:10.1038/s41579-019-0250-1

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