Unlike biologically available nitrogen and phosphorus, which are often at limiting concentrations in surface seawater, sulfur in the form of sulfate is plentiful and not considered to constrain marine microbial activity. Nonetheless, in a model system in which a marine bacterium obtains all of its carbon from co-cultured phytoplankton, bacterial gene expression suggests that at least seven dissolved organic sulfur (DOS) metabolites support bacterial heterotrophy. These labile exometabolites of marine dinoflagellates and diatoms include taurine, N-acetyltaurine, isethionate, choline-O-sulfate, cysteate, 2,3-dihydroxypropane-1-sulfonate (DHPS), and dimethylsulfoniopropionate (DMSP). Leveraging from the compounds identified in this model system, we assessed the role of sulfur metabolites in the ocean carbon cycle by mining the Tara Oceans dataset for diagnostic genes. In the 1.4 million bacterial genome equivalents surveyed, estimates of the frequency of genomes harboring the capability for DOS metabolite utilization ranged broadly, from only 1 out of every 190 genomes (for the C2 sulfonate isethionate) to 1 out of every 5 (for the sulfonium compound DMSP). Bacteria able to participate in DOS transformations are dominated by Alphaproteobacteria in the surface ocean, but by SAR324, Acidimicrobiia, and Gammaproteobacteria at mesopelagic depths, where the capability for utilization occurs in higher frequency than in surface bacteria for more than half the sulfur metabolites. The discovery of an abundant and diverse suite of marine bacteria with the genetic capacity for DOS transformation argues for an important role for sulfur metabolites in the pelagic ocean carbon cycle.
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Fuhrman JA. Marine viruses and their biogeochemical and ecological effects. Nature. 1999;399:541.
Morán XAG, Ducklow HW, Erickson M. Carbon fluxes through estuarine bacteria reflect coupling with phytoplankton. Mar Ecol Prog Ser. 2013;489:75–85.
Hansell DA. Recalcitrant dissolved organic carbon fractions. Ann Rev Marine Sci. 2013;5:421–45. https://doi.org/10.1146/annurev-marine-120710-100757.
Dupont CL, Rusch DB, Yooseph S, Lombardo M-J, Richter RA, Valas R, et al. Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME J. 2012;6:1186–99.
Tripp HJ, Kitner JB, Schwalbach MS, Dacey JW, Wilhelm LJ, Giovannoni SJ. SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature. 2008;452:741–4. https://doi.org/10.1038/nature06776.
Sunda W, Kieber D, Kiene R, Huntsman S. An antioxidant function for DMSP and DMS in marine algae. Nature. 2002;418:317–20.
Strom S, Wolfe G, Slajer A, Lambert S, Clough J. Chemical defense in the microplankton II: inhibition of protist feeding by beta-dimethylsulfoniopropionate (DMSP). Limnol Oceanogr. 2003;48:230–7.
Kiene RP, Linn LJ, Bruton JA. New and important roles for DMSP in marine microbial communities. J Sea Res. 2000;43:209–24.
Kaiser K, Benner R. Organic matter transformations in the upper mesopelagic zone of the North Pacific: chemical composition and linkages to microbial community structure. J Geophys Res Oceans. 2012;C10123:117.
Mopper K, Schultz CA, Chevolot L, Germain C, Revuelta R, Dawson R. Determination of sugars in unconcentrated seawater and other natural waters by liquid chromatography and pulsed amperometric detection. Environ Sci Technol. 1992;26:133–8.
Azam F, Malfatti F. Microbial structuring of marine ecosystems. Nat Rev Microbiol. 2007;5:782–91. https://doi.org/10.1038/nrmicro1747.
McCarren J, Becker JW, Repeta DJ, Shi Y, Young CR, Malmstrom RR, et al. Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci USA. 2010;107:16420–7. https://doi.org/10.1073/pnas.1010732107.
Poretsky RS, Sun S, Mou X, Moran MA. Transporter genes expressed by coastal bacterioplankton in response to dissolved organic carbon. Environ Microbiol. 2010;12:616–27. https://doi.org/10.1111/j.1462-2920.2009.02102.x.
Satinsky BM, Crump BC, Smith CB, Sharma S, Zielinski BL, Doherty M, et al. Microspatial gene expression patterns in the Amazon River Plume. Proc Natl Acad Sci USA. 2014;111:11085–90.
Landa M, Burns AS, Roth SJ, Moran MA. Bacterial transcriptome remodeling during sequential co-culture with a marine dinoflagellate and diatom. ISME J. 2017;11:2677–90.
Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, et al. Structure and function of the global ocean microbiome. Science. 2015;348:1261359.
Kiene RP, Service SK. Decomposition of dissolved DMSP and DMS in estuarine waters: dependence on temperature and substrate concentration. Mar Ecol Prog Ser. 1991;76:1–11.
Stewart FJ, Ottesen EA, DeLong EF. Development and quantitative analyses of a universal rRNA-subtraction protocol for microbial metatranscriptomics. ISME J. 2010;4:896–907.
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9.
Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–9.
Wagner GP, Kin K, Lynch VJ. Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory Biosci. 2012;131:281–5.
Love M, Anders S, Huber W. Differential analysis of count data—the DESeq2 package. Genome Biol. 2014;15:550.
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D et al. vegan: Community Ecology Package. 2017. https://CRAN.R-project.org/package=vegan.
Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using Diamond. Nat Methods. 2014;12:59–60.
Busby WF. Sulfopropanedial and cysteinolic acid in the diatom. Biochim Biophys Acta. 1966;121:160–1.
Busby WF, Benson AA. Sulfonic acid metabolism in the diatom Navicula pelliculosa. Plant Cell Physiol. 1973;14:1123–32.
Durham BP, Sharma S, Luo H, Smith CB, Amin SA, Bender SJ, et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proc Natl Acad Sci USA. 2015;112:453–7. https://doi.org/10.1073/pnas.1413137112.
Mayer J, Huhn T, Habeck M, Denger K, Hollemeyer K, Cook AM. 2, 3-Dihydroxypropane-1-sulfonate degraded by Cupriavidus pinatubonensis JMP134: purification of dihydroxypropanesulfonate 3-dehydrogenase. Microbiology. 2010;156:1556–64.
Shibuya I, Yagi T, Benson AA. In Japanese Society of Plant Physiologists, editor. Studies on microalgae and photosynthetic bacteria. Tokyo: University of Tokyo Press; 1963. p. 627–36.
Denger K, Lehmann S, Cook AM. Molecular genetics and biochemistry of N-acetyltaurine degradation by Cupriavidus necator H16. Microbiology. 2011;157:2983–91.
Gorzynska AK, Denger K, Cook AM, Smits TH. Inducible transcription of genes involved in taurine uptake and dissimilation by Silicibacter pomeroyi DSS-3T. Arch Microbiol. 2006;185:402.
Weinitschke S, Sharma PI, Stingl U, Cook AM, Smits TH. Gene clusters involved in isethionate degradation by terrestrial and marine bacteria. Appl Environ Microbiol. 2010;76:618–21.
Jackson AE, Ayer SW, Laycock MV. The effect of salinity on growth and amino acid composition in the marine diatom Nitzschia pungens. Can J Bot. 1992;70:2198–201.
Boroujerdi AF, Lee PA, DiTullio GR, Janech MG, Vied SB, Bearden DW. Identification of isethionic acid and other small molecule metabolites of Fragilariopsis cylindrus with nuclear magnetic resonance. Anal Bioanal Chem. 2012;404:777–84.
Lidbury I, Kimberley G, Scanlan DJ, Murrell JC, Chen Y. Comparative genomics and mutagenesis analyses of choline metabolism in the marine Roseobacter clade. Environ Microbiol. 2015;17:5048–62.
Ikawa M, Taylor RF. In Martin D, Padilla G, editors. Marine pharmacognosy. Choline and related substances in algae. New York: Academic Press; 1973. p. 203–40.
Taylor RF, Ikawa M, Sasner JJ Jr, Thurberg FP, Andersen KK. Occurrence of choline esters in the marine dionflagellate Amphidinium carteri. J Phycol. 1974;10:279–83.
Kiene RP, Linn LJ, González J, Moran MA, Bruton JA. Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine bacterioplankton. Appl Environ Microbiol. 1999;65:4549–58.
Keller MD, Bellows WK, Guillard RR. In Saltzman ES, Cooper WJ, editors. Biogenic sulfur in the environment. Dimethyl sulfide production in marine phytoplankton. Washington D.C.: ACS Publications; 1989. p. 167–82.
Curson AR, Todd JD, Sullivan MJ, Johnston AW. Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat Rev Microbiol. 2011;9:849.
Simó R. Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends Ecol Evol. 2001;16:287–94.
Moran MA, Reisch CR, Kiene RP, Whitman WB. Genomic insights into bacterial DMSP transformations. Annu Rev Mar Sci. 2012;4:523–42.
Eyice Ö, Schäfer H. Culture-dependent and culture-independent methods reveal diverse methylotrophic communities in terrestrial environments. Arch Microbiol. 2016;198:17–26.
Suylen G, Large P, Van Dijken J, Kuenen J. Methyl mercaptan oxidase, a key enzyme in the metabolism of methylated sulphur compounds by Hyphomicrobium EG. Microbiology. 1987;133:2989–97.
Eyice Ö, Myronova N, Pol A, Carrión O, Todd JD, Smith TJ, et al. Bacterial SBP56 identified as a Cu-dependent methanethiol oxidase widely distributed in the biosphere. ISME J. 2017;12:145.
González JM, Kiene RP, Moran MA. Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class proteobacteria. Appl Environ Microbiol. 1999;65:3810–9.
Todd JD, Curson AR, Sullivan MJ, Kirkwood M, Johnston AW. The Ruegeria pomeroyi acuI gene has a role in DMSP catabolism and resembles yhdH of E. coli and other bacteria in conferring resistance to acrylate. PLoS ONE. 2012;7:e35947.
Varaljay VA, Robidart J, Preston CM, Gifford SM, Durham BP, Burns AS, et al. Single-taxon field measurements of bacterial gene regulation controlling DMSP fate. ISME J. 2015;9:1677–86.
Lehmann S. Sulfite dehydrogenases in organotrophic bacteria: enzymes, genes and regulation. Konstanz, Germany: University of Konstanz; 2013.
Lenk S, Moraru C, Hahnke S, Arnds J, Richter M, Kube M, et al. Roseobacter clade bacteria are abundant in coastal sediments and encode a novel combination of sulfur oxidation genes. ISME J. 2012;6:2178–87.
Denger K, Smits TH, Cook AM. l-Cysteate sulpho-lyase, a widespread pyridoxal 5′-phosphate-coupled desulphonative enzyme purified from Silicibacter pomeroyi DSS-3T. Biochem J. 2006;394:657–64.
Reisch CR, Crabb WM, Gifford SM, Teng Q, Stoudemayer MJ, Moran MA, et al. Metabolism of dimethylsulphoniopropionate by Ruegeria pomeroyi DSS‐3. Mol Microbiol. 2013;89:774–91.
Lei L, Cherukuri KP, Alcolombri U, Meltzer D, Tawfik DS. The dimethylsulfoniopropionate (DMSP) lyase and lyase-like cupin family consists of bona fide DMSP lyases as well as other enzymes with unknown function. Biochemistry. 2018;57:3364–77.
Curson AR, Williams BT, Pinchbeck BJ, Sims LP, Martínez AB, Rivera PPL, et al. DSYB catalyses the key step of dimethylsulfoniopropionate biosynthesis in many phytoplankton. Nat Microbiol. 2018;3:430.
Galí M, Devred E, Levasseur M, Royer S-J, Babin M. A remote sensing algorithm for planktonic dimethylsulfoniopropionate (DMSP) and an analysis of global patterns. Remote Sens Environ. 2015;171:171–84.
Stefels J. Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res. 2000;43:183–97.
Denger K, Weiss M, Felux A-K, Schneider A, Mayer C, Spiteller D, et al. Sulphoglycolysis in Escherichia coli K-12 closes a gap in the biogeochemical sulphur cycle. Nature. 2014;507:114–7.
Saidha T, Stern AI, Schiff JA. Taurine conjugates in the lipid fraction of Euglena cells and their mitochondria. Microbiology. 1993;139:251–7.
Clifford EL, Hansell DA, Varela MM, Nieto‐Cid M, Herndl GJ, Sintes E. Crustacean zooplankton release copious amounts of dissolved organic matter as taurine in the ocean. Limnol Oceanogr. 2017;62:2745–58.
Thume K, Gebser B, Chen L, Meyer N, Kieber DJ & Pohnert G. The metabolite dimethylsulfoxonium propionate extends the marine organosulfur cycle. Nature. 2018. https://doi.org/10.1038/s41586-018-0675-0.
Ksionzek KB, Lechtenfeld OJ, McCallister SL, Schmitt-Kopplin P, Geuer JK, Geibert W, et al. Dissolved organic sulfur in the ocean: Biogeochemistry of a petagram inventory. Science. 2016;354:456–9.
Howard EC, Henriksen JR, Buchan A, Reisch CR, Bürgmann H, Welsh R, et al. Bacterial taxa that limit sulfur flux from the ocean. Science. 2006;314:649–52.
Reisch CR, Stoudemayer MJ, Varaljay VA, Amster IJ, Moran MA, Whitman WB. Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria. Nature. 2011;473:208–11.
Bullock HA, Reisch CR, Burns AS, Moran MA, Whitman WB. Regulatory and functional diversity of methylmercaptopropionate coenzyme A ligases from the dimethylsulfoniopropionate demethylation pathway in Ruegeria pomeroyi DSS-3 and other proteobacteria. J Bacteriol. 2014;196:1275–85.
Wirth JS. Phylogenomics and the metabolism of sulfur compounds in the Roseobacter group. Athens, GA, USA: University of Georgia; 2019.
Todd JD, Kirkwood M, Newton-Payne S, Johnston AW. DddW, a third DMSP lyase in a model Roseobacter marine bacterium, Ruegeria pomeroyi DSS-3. ISME J. 2012;6:223–6.
Todd JD, Rogers R, Li YG, Wexler M, Bond PL, Sun L, et al. Structural and regulatory genes required to make the gas dimethyl sulfide in bacteria. Science. 2007;315:666–9.
Todd J, Curson A, Dupont C, Nicholson P, Johnston A. The dddP gene, encoding a novel enzyme that converts dimethylsulfoniopropionate into dimethyl sulfide, is widespread in ocean metagenomes and marine bacteria and also occurs in some Ascomycete fungi. Environ Microbiol. 2009;11:1376–85.
Todd JD, Curson AR, Kirkwood M, Sullivan MJ, Green RT, Johnston AW. DddQ, a novel, cupin‐containing, dimethylsulfoniopropionate lyase in marine roseobacters and in uncultured marine bacteria. Environ Microbiol. 2011;13:427–38.
Brüggemann C, Denger K, Cook AM, Ruff J. Enzymes and genes of taurine and isethionate dissimilation in Paracoccus denitrificans. Microbiology. 2004;150:805–16.
We appreciate assistance from C Smith and S Roth, and thank N Ivanova for help with IMG database access. Computing resources and technical expertise were provided by the Georgia Genomics and Bioinformatics Core. This work was funded by NSF grants OCE-1342694, OCE-1342699, IOS-1656311 and The Gordon and Betty Moore Foundation grant #5503. This research used resources of the Joint Genome Institute (JGI) and the National Energy Research Scientific Computing Center (NERSC), US Department of Energy Office of Science User Facilities operated under Contract No. DE-AC02-05CH11231.
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