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Sulfur Metabolites in the Pelagic Ocean

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Sulfur Metabolites in the Pelagic Ocean REVIEWS Sulfur metabolites in the pelagic ocean Mary Ann Moran 1* and Bryndan P. Durham 2,3 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. 2− osmolytes6 7 Allelochemicals Inorganic sulfur in the form of sulfate (SO4 ) has one of as cell and redox buffers . According to the Chemicals produced by a the highest concentrations of any dissolved consti tuent canonical elemental ratio of ocean plankton biomass living organism that can be (REF.8) in seawater (~28 mM), indicative of it being a major (C124N16P1S1.3) , one atom of sulfur needs to be beneficial or detrimental to component of marine salt. From this massive reservoir, assimilated into marine microbial biomass for every another organism. sulfur is taken up by marine microorganisms and syn­ 95 atoms of carbon assimilated. Volatile thesized into a variety of organic molecules. Eventually, Although the inorganic sulfur reservoir in seawater A molecule that readily most microbially produced organic sulfur is reminera­ greatly exceeds microbial sulfur quotas, the conversion vaporizes into air. lized and the oxidized sulfur atom returned to the sulfate of sulfate (S oxidation state +6) to cysteine (S oxidation reservoir. In between, however, it plays central roles in state −2) requires an eight­electron reduction. Producing Metabolites Small molecules that are a the biology of marine microorganisms and the food webs fully reduced sulfur from sulfate has an energy cost −1 direct product of metabolism. they sustain, by functioning in metabolism, contributing to microorganisms of 1,815 kJ mol , as compared to to membrane structure, supporting osmotic and redox 605 kJ mol−1 for producing fully reduced carbon from Aerosols balance, and acting as allelochemicals and signalling mol­ CO (REF.9). The expense of sulfate reduction is not usu­ Suspensions of solid or liquid 2 volatile particles in gas. ecules. Some marine microorganisms synthesize ally prohibitive for the photosynthetic phytoplankton in sulfur metabolites, and a fraction of these escape across the sunlit ocean. Bacterioplankton, on the other hand, Cloud nucleation the air–sea interface. Despite the small absolute amount, are often energy­ limited, and therefore sulfur that has Formation of aerosol particles this is the largest natural source of sulfur that is released already been reduced and incorporated into organic on which water vapour into the atmosphere. Following oxidation, ocean­derived matter is a valuable commodity. Bacteria can obtain condenses in the first step aerosols of cloud formation. sulfur influences the acid–base balance of and pre­ reduced sulfur from the seawater dissolved organic rainwater and affects cloud nucleation at a global scale1–3. sulfur (DOS) pool, into which labile organic sulfur 1Department of Marine Sulfur metabolite cycling begins when micro­ compounds are released from phytoplankton and other Sciences, University of organisms acquire and reduce sulfate from seawater, marine microorganisms. Two widespread marine bacte­ Georgia, Athens, GA, USA. a straightforward process for most. The assimilatory rial taxa, the proteobacterial groups SAR11 and SAR86, 2School of Oceanography, sulfate reduction pathway that converts readily availa­ have actually lost the sulfate assimilation pathway and University of Washington, Seattle, WA, USA. ble sulfate to sulfide (H2S) for incorporation into organic instead are wholly reliant on scavenging reduced sulfur molecules is nearly ubiquitous in marine phytoplankton from seawater10,11. 3Department of Biology, biosynthesis University of Florida, and bacterioplankton. Once reduced, sulfur is converted The assimilation of sulfur for molecular Gainesville, FL, USA. into the essential amino acids methionine and cysteine, is one example of the accumulating evidence from both *e- mail: [email protected] into cofactors such as biotin and S­adenosylmethionine biological and chemical perspectives of a decidedly 4 5 https://doi.org/10.1038/ and into microbial sulfolipid and taurolipid mem­ active role for sulfur metabolite pools in the aerobic s41579-019-0250-1 branes. Sulfur­ containing metabolites also function ocean. These recent discoveries (and rediscoveries) NATURE REVIEWS | MICROBIOLOGY REVIEWS Osmolytes include the identification of a diverse suite of sulfur-​ The DOS in this last category includes molecules made Organic molecules used by containing molecules synthesized by marine phy­ more resistant to bacterial processing from biological organisms to maintain cellular toplankton12–14, characterization of numerous genes and chemical transformations23. What is unmistaka­ water balance. mediating DOS metabolism in cultured and uncul­ ble from this rough budget, and what can change only 14–19 Assimilation tured marine microorganisms , and recognition of modestly as more information becomes available, is that Process by which organisms the unique biogeochemical roles of DOS in the ocean’s the vast majority of phytoplankton­ produced organic transform compounds into microbial network6,20. In this Review, we examine sulfur sulfur released into seawater is rapidly processed and organic molecules. metabolites, defined as sulfur­ containing organic mole­ returned to an inorganic form by ocean bacteria24. cules that are direct products of metabolism, that are Because the sulfur metabolites travel through the Biosynthesis The process by which synthesized and catabolized by marine microorganisms ocean’s organic matter reservoirs attached to carbon organisms assemble the in the pelagic ocean, and explore how they function as molecules, microbial processing represents a link components of molecules. ecological links between ocean microorganisms. between the marine carbon and sulfur cycles. There are suggestions that this linkage may not always have tight Biogeochemical Organic sulfur cycling in the ocean stoichiometry Relating to the cycling of , with DOS molecules being cycled more elements through biological, An estimated 1,320 Tg of sulfur is fixed by marine phyto­ rapidly than the bulk dissolved organic carbon (DOC) geological and chemical plankton into organic material annually20, of which pool. Some coastal bacterioplankton communities have processes. ~600 Tg is subsequently released into seawater as DOS been shown to preferentially process organic sulfur by various biological processes (Fig. 1). The majority of from DOC, assimilating organic matter with a 1.6­fold Tg 25 Teragram, 1012 grams. these phytoplankton-​derived metabolites are taken up bias towards sulfur­ containing molecules . Similarly, from the DOS pool by marine bacteria on short times­ bulk elemental measures of surface ocean particulate Stoichiometry cales (minutes to days)6,21,22. The more reduced the sulfur organic matter compared to depth­ integrated values A quantitative measure of the atom is in DOS compared to sulfate, the more readily it and in situ sulfur assimilation rates indicate selective relationship among elements in a chemical compound. can be incorporated into cellular material, and the more consumption of newly synthesized organic sulfur in energy it yields for bacteria when oxidized back to sul­ the upper water column26. The sulfur­ rich compound Turnover times fate. A fraction of the DOS pool (~25 Tg) is volatile and dimethylsulfoniopropionate (DMSP), with a C:S ratio of The times required to effluxes to the atmosphere (~4% of annual DOS inputs), 5:1, is the most significant single bacterioplankton sub­ completely renew the content whereas another ~1 Tg of DOS (0.2%) becomes part of strate so far identi fied, having high flux rates and very of reservoirs. the ocean’s non­ labile dissolved organic matter pool, fast turnover times in surface seawater6,27. Deeper in the with an estimated average lifetime of ~4,000 years20. ocean (1,000–5,000 m), the DOC­to ­DOS ratios increase Air–sea Remineralization exchange Particulate a 574 Tg S per yeard 25 Tg S per year Sulfatea 4 organic sulfur 3 (bacteria)a 1.2 × 1012 Tg S 62 Tg S Net primary 6 1 production a 1,320 Tg S per year • Exudation 7 • Senescence • Lysis Organic sulfur 2 600 Tg S per yearb (phytoplankton)a Dissolved organic sulfur metabolites 28 Tg S 24 Tg Sa b Grazing Dissolved 5 1 Tg S per yearc 720 Tg S per year organic sulfur (total)a Microbial Removal 6,700 Tg S carbon pump Particulate organic 1 Tg S per yeara sulfur (other) Fig. 1 | Organic
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