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  • Review Article
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Sulfur metabolites in the pelagic ocean

Nature Reviews Microbiology volume 17, pages 665–678 (2019)Cite this article

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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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References

  1. Andreae, M. O. Ocean-atmosphere interactions in the global biogeochemical sulfur cycle. Mar. Chem. 30, 1–29 (1990).

    Article  CAS  Google Scholar 

  2. Malin, G. in Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds (eds Kiene, R. P., Visscher, P. T., Keller, M. D. & Kirst, G. O.) 177–189 (Springer, 1996).

  3. Quinn, P. & Bates, T. The case against climate regulation via oceanic phytoplankton sulphur emissions. Nature 480, 51 (2011).

    Article  CAS  PubMed  Google Scholar 

  4. Cook, A. M., Smits, T. H. & Denger, K. in Microbial Sulfur Metabolism (eds Dahl, C. & Friedrich, C. G.) 170–183 (Springer, 2008).

  5. Batrakov, S. G., Nikitin, D. I. & Pitryuk, I. A. A novel glycolipid, 1, 2-diacyl-3-α-glucuronopyranosyl-sn-glycerol taurineamide, from the budding seawater bacterium Hyphomonas jannaschiana. Biochim. Biophys. Acta Lipids Lipid Metab. 1302, 167–176 (1996).

    Article  Google Scholar 

  6. Kiene, R. P., Linn, L. J. & Bruton, J. A. New and important roles for DMSP in marine microbial communities. J. Sea Res. 43, 209–224 (2000). This review provides biological, chemical and ecological perspectives on the myriad roles of a well-studied sulfur metabolite, DMSP.

    Article  CAS  Google Scholar 

  7. Loi, V. V., Rossius, M. & Antelmann, H. Redox regulation by reversible protein S-thiolation in bacteria. Front. Microbiol. 6, 187 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Ho, T. Y. et al. The elemental composition of some marine phytoplankton 1. J. Phycol. 39, 1145–1159 (2003).

    Article  CAS  Google Scholar 

  9. Giordano, M. & Raven, J. A. Nitrogen and sulfur assimilation in plants and algae. Aquat. Bot. 118, 45–61 (2014).

    Article  CAS  Google Scholar 

  10. Dupont, C. L. et al. Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME J. 6, 1186–1199 (2012). This early example of scientific discovery through assembling genomes from metagenomes uncovers unique biogeochemical requirements in an uncultured taxon of marine bacteria.

    Article  CAS  PubMed  Google Scholar 

  11. Tripp, H. J. et al. SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452, 741–744 (2008).

    Article  CAS  PubMed  Google Scholar 

  12. Busby, W. F. Sulfopropanediol and cysteinolic acid in the diatom. Biochem. Biophys. Acta 121, 160–161 (1966).

    Article  CAS  PubMed  Google Scholar 

  13. Busby, W. F. & Benson, A. A. Sulfonic acid metabolism in the diatom Navicula pelliculosa. Plant Cell Physiol. 14, 1123–1132 (1973).

    CAS  Google Scholar 

  14. Durham, B. P. et al. Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria in the surface ocean. Nat. Microbiol. https://doi.org/10.1038/s41564-019-0507-5 (2019). The distribution and abundance of C2 and C3 sulfonates are described in eukaryotic phytoplankton metabolomes, and a biosynthetic pathway is proposed.

  15. Alcolombri, U. et al. Identification of the algal dimethyl sulfide–releasing enzyme: a missing link in the marine sulfur cycle. Science 348, 1466–1469 (2015).

    Article  CAS  PubMed  Google Scholar 

  16. Denger, K., Lehmann, S. & Cook, A. M. Molecular genetics and biochemistry of N-acetyltaurine degradation by Cupriavidus necator H16. Microbiology 157, 2983–2991 (2011).

    Article  CAS  PubMed  Google Scholar 

  17. Howard, E. C. et al. Bacterial taxa that limit sulfur flux from the ocean. Science 314, 649–652 (2006).

    Article  CAS  PubMed  Google Scholar 

  18. Mayer, J. et al. 2, 3-Dihydroxypropane-1-sulfonate degraded by Cupriavidus pinatubonensis JMP134: purification of dihydroxypropanesulfonate 3-dehydrogenase. Microbiology 156, 1556–1564 (2010). Bacterial genes and pathways for transforming sulfur metabolites are discovered in this example of how the foundation of our current understanding of organic sulfur processing in natural environments was built.

    Article  CAS  PubMed  Google Scholar 

  19. Curson, A. R., Todd, J. D., Sullivan, M. J. & Johnston, A. W. Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat. Rev. Microbiol. 9, 849 (2011).

    Article  CAS  PubMed  Google Scholar 

  20. Ksionzek, K. B. et al. Dissolved organic sulfur in the ocean: Biogeochemistry of a petagram inventory. Science 354, 456–459 (2016). This study provides a stoichiometric analysis of the marine pool of non-labile dissolved organic matter that reveals selective removal of sulfur compared to bulk carbon.

    Article  CAS  PubMed  Google Scholar 

  21. González, J. M., Kiene, R. P. & Moran, M. A. Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class Proteobacteria. Appl. Environ. Microbiol. 65, 3810–3819 (1999).

    PubMed  PubMed Central  Google Scholar 

  22. Landa, M. et al. Sulfur metabolites that facilitate oceanic phytoplankton-bacteria carbon flux. ISME J. https://doi.org/10.1038/s41396-019-0455-3 (2019). A diversity of diatom-derived and dinoflagellate-derived sulfur metabolites are shown to support heterotrophic bacterial growth.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Jiao, N. et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593 (2010).

    Article  CAS  PubMed  Google Scholar 

  24. Koch, B. P. et al. Response to comment on “Dissolved organic sulfur in the ocean: biogeochemistry of a petagram inventory”. Science 356, 813 (2017).

    Article  CAS  PubMed  Google Scholar 

  25. Vorobev, A. et al. Identifying labile DOM components in a coastal ocean through depleted bacterial transcripts and chemical signals. Environ. Microbiol. 20, 3012–3030 (2018).

    Article  CAS  PubMed  Google Scholar 

  26. Bates, T. S. et al. The cycling of sulfur in surface seawater of the northeast Pacific. J. Geophys. Res. Oceans 99, 7835–7843 (1994).

    Article  CAS  Google Scholar 

  27. Ledyard, K. M. & Dacey, J. W. Microbial cycling of DMSP and DMS in coastal and oligotrophic seawater. Limnol. Oceanogr. 41, 33–40 (1996).

    Article  CAS  Google Scholar 

  28. Archer, S. D., Widdicombe, C. E., Tarran, G. A., Rees, A. P. & Burkill, P. H. Production and turnover of particulate dimethylsulphoniopropionate during a coccolithophore bloom in the northern North Sea. Aquat. Microb. Ecol. 24, 225–241 (2001).

    Article  Google Scholar 

  29. 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. 171, 171–184 (2015).

    Article  Google Scholar 

  30. Stefels, J. & van Leeuwe, M. A. Effects of iron and light stress on the biochemical composition of Antarctic Phaeocystis sp. (Prymnesiophyceae): I. Intracellular DMSP concentrations. J. Phycol. 34, 486–495 (1998).

    Article  CAS  Google Scholar 

  31. Steinke, M., Wolfe, G. V. & Kirst, G. O. Partial characterisation of dimethylsulfoniopropionate (DMSP) lyase isozymes in 6 strains of Emiliania huxleyi. Mar. Ecol. Progr. Ser. 175, 215–225 (1998).

    Article  CAS  Google Scholar 

  32. Gebser, B. & Pohnert, G. Synchronized regulation of different zwitterionic metabolites in the osmoadaption of phytoplankton. Mar. Drugs 11, 2168–2182 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nakamura, H., Fujimaki, K., Sampei, O. & Murai, A. Gonyol: methionine-induced sulfonium accumulation in a dinoflagellate Gonyaulax polyedra. Tetrahedron Lett. 34, 8481–8484 (1993).

    Article  CAS  Google Scholar 

  34. Thume, K. et al. The metabolite dimethylsulfoxonium propionate extends the marine organosulfur cycle. Nature 563, 412–415 (2018). A novel sulfoxonium compound is characterized in marine plankton, revealing a new component of the marine sulfur metabolite pool.

    Article  CAS  PubMed  Google Scholar 

  35. Bisseret, P. et al. Occurrence of phosphatidylsulfocholine, the sulfonium analog of phosphatidylcholine in some diatoms and algae. Biochim. Biophys. Acta Lipids Lipid Metab. 796, 320–327 (1984).

    Article  CAS  Google Scholar 

  36. Jefferson, A., Tanner, D., Eisele, F. & Berresheim, H. Sources and sinks of H2SO4 in the remote Antarctic marine boundary layer. J. Geophys. Res. Atmos. 103, 1639–1645 (1998).

    Article  CAS  Google Scholar 

  37. Kelly, D. P. & Murrell, J. C. Microbial metabolism of methanesulfonic acid. Arch. Microbiol. 172, 341–348 (1999).

    Article  CAS  Google Scholar 

  38. Biller, S. J. et al. Bacterial vesicles in marine ecosystems. Science 343, 183–186 (2014).

    Article  CAS  PubMed  Google Scholar 

  39. Saidha, T., Stern, A. I. & Schiff, J. A. Taurine conjugates in the lipid fraction of Euglena cells and their mitochondria. Microbiology 139, 251–257 (1993).

    CAS  Google Scholar 

  40. Moran, M. A., Reisch, C. R., Kiene, R. P. & Whitman, W. B. Genomic insights into bacterial DMSP transformations. Annu. Rev. Mar. Sci. 4, 523–542 (2012).

    Article  Google Scholar 

  41. Johnson, W. M., Soule, M. C. K. & Kujawinski, E. B. Extraction efficiency and quantification of dissolved metabolites in targeted marine metabolomics. Limnol. Oceanogr. Meth. 15, 417–428 (2017). The limitations of current chemical methods for measuring polar metabolites in a seawater matrix are systematically examined.

    Article  Google Scholar 

  42. Gao, Y., Schofield, O. M. & Leustek, T. Characterization of sulfate assimilation in marine algae focusing on the enzyme 5′-adenylylsulfate reductase. Plant Physiol. 123, 1087–1096 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Matrai, P. & Keller, M. Total organic sulfur and dimethylsulfoniopropionate in marine phytoplankton: intracellular variations. Mar. Biol. 119, 61–68 (1994).

    Article  CAS  Google Scholar 

  44. Curson, A. R. et al. Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process. Nat. Microbiol. 2, 17009 (2017).

    Article  CAS  PubMed  Google Scholar 

  45. Curson, A. R. et al. DSYB catalyses the key step of dimethylsulfoniopropionate biosynthesis in many phytoplankton. Nat. Microbiol. 3, 430 (2018). In Curson et al. (2017, 2018), the first DMSP biosynthetic gene DSYB is experimentally demonstrated in eukaryotic phytoplankton.

    Article  CAS  PubMed  Google Scholar 

  46. Gage, D. A. et al. A new route for synthesis of dimethylsulphoniopropionate in marine algae. Nature 387, 891 (1997).

    Article  CAS  PubMed  Google Scholar 

  47. Kocsis, M. G. & Hanson, A. D. Biochemical evidence for two novel enzymes in the biosynthesis of 3-dimethylsulfoniopropionate in Spartina alterniflora. Plant Physiol. 123, 1153–1162 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Liao, C. & Seebeck, F. P. In vitro reconstitution of bacterial DMSP biosynthesis. Angew. Chem. 131, 3591–3594 (2019).

    Article  Google Scholar 

  49. Rhodes, D., Gage, D. A., Cooper, A. J. & Hanson, A. D. S-Methylmethionine conversion to dimethylsulfoniopropionate: evidence for an unusual transamination reaction. Plant Physiol. 115, 1541–1548 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Kitaguchi, H., Uchida, A. & Ishida, Y. Purification and characterization of L-methionine decarboxylase from Crypthecodinium cohnii. Fish Sci. 65, 613–617 (1999).

    Article  CAS  Google Scholar 

  51. Uchida, A. et al. in Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds (eds Kiene, R. P., Visscher, P. T., Keller, M. D. & Kirst, G. O.) 97–107 (Springer, 1996).

  52. Benson, A., Cook, J. & Yagi, T. Sulfoquinovose metabolism studies. Plant Physiol. 37 (Suppl.), xliv (1962).

  53. Benning, C. & Somerville, C. Identification of an operon involved in sulfolipid biosynthesis in Rhodobacter sphaeroides. J. Bacteriol. 174, 6479–6487 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Benning, C. & Somerville, C. Isolation and genetic complementation of a sulfolipid-deficient mutant of Rhodobacter sphaeroides. J. Bacteriol. 174, 2352–2360 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Rossak, M., Tietje, C., Heinz, E. & Benning, C. Accumulation of UDP-sulfoquinovose in a sulfolipid-deficient mutant of Rhodobacter sphaeroides. J. Biol. Chem. 270, 25792–25797 (1995). The genes required for the biosynthesis of sulfolipid are first identified here in a photosynthetic bacterium.

    Article  CAS  PubMed  Google Scholar 

  56. Güler, S., Essigmann, B. & Benning, C. A cyanobacterial gene, sqdX, required for biosynthesis of the sulfolipid sulfoquinovosyldiacylglycerol. J. Bacteriol. 182, 543–545 (2000).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Sanda, S., Leustek, T., Theisen, M. J., Garavito, R. M. & Benning, C. Recombinant Arabidopsis SQD1 converts UDP-glucose and sulfite to the sulfolipid head group precursor UDP-sulfoquinovose in vitro. J. Biol. Chem. 276, 3941–3946 (2001).

    Article  CAS  PubMed  Google Scholar 

  58. Yu, B., Xu, C. & Benning, C. Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc. Natl Acad. Sci. USA 99, 5732–5737 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Agnello, G., Chang, L. L., Lamb, C. M., Georgiou, G. & Stone, E. M. Discovery of a substrate selectivity motif in amino acid decarboxylases unveils a taurine biosynthesis pathway in prokaryotes. ACS Chem. Biol. 8, 2264–2271 (2013).

    Article  CAS  PubMed  Google Scholar 

  60. Amin, S. et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98 (2015).

    Article  CAS  PubMed  Google Scholar 

  61. Tevatia, R. et al. The taurine biosynthetic pathway of microalgae. Algal Res. 9, 21–26 (2015).

    Article  Google Scholar 

  62. Keller, M. D. Dimethyl sulfide production and marine phytoplankton: the importance of species composition and cell size. Biol. Oceanogr. 6, 375–382 (1989).

    Google Scholar 

  63. Landa, M., Burns, A. S., Roth, S. J. & Moran, M. A. Bacterial transcriptome remodeling during sequential co-culture with a marine dinoflagellate and diatom. ISME J. 11, 2677–2690 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Lønborg, C., Middelboe, M. & Brussaard, C. P. Viral lysis of Micromonas pusilla: impacts on dissolved organic matter production and composition. Biogeochemistry 116, 231–240 (2013).

    Article  CAS  Google Scholar 

  65. Nagata, T. & Kirchman, D. L. Release of macromolecular organic complexes by heterotrophic marine flagellates. Mar. Ecol. Progr. Ser. 83, 233–240 (1992).

    Article  CAS  Google Scholar 

  66. Thornton, D. C. Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean. Eur. J. Phycol. 49, 20–46 (2014).

    Article  CAS  Google Scholar 

  67. Ruiz-González, C. et al. Sunlight effects on the osmotrophic uptake of DMSP-sulfur and leucine by polar phytoplankton. PLOS ONE 7, e45545 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Spiese, C. E., Sanford, J. L., Bowling, M. N., Tatarkov, E. A. & Pinkney, A. L. Methanesulfonate supports growth as the sole sulfur source for the marine diatom Thalassiosira pseudonana NCMA 1335. Aquat. Microb. Ecol. 78, 177–185 (2017).

    Article  Google Scholar 

  69. Vila-Costa, M. et al. Dimethylsulfoniopropionate uptake by marine phytoplankton. Science 314, 652–654 (2006).

    Article  CAS  PubMed  Google Scholar 

  70. Zubkov, M. V., Tarran, G. A. & Fuchs, B. M. Depth related amino acid uptake by Prochlorococcus cyanobacteria in the Southern Atlantic tropical gyre. FEMS Microbiol. Ecol. 50, 153–161 (2004).

    Article  CAS  PubMed  Google Scholar 

  71. Reisch, C. R. et al. Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria. Nature 473, 208 (2011).

    Article  CAS  PubMed  Google Scholar 

  72. Eyice, Ö. et al. Bacterial SBP56 identified as a Cu-dependent methanethiol oxidase widely distributed in the biosphere. ISME J. 12, 145 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Reisch, C. R., Moran, M. A. & Whitman, W. B. Bacterial catabolism of dimethylsulfoniopropionate (DMSP). Front. Microbiol. 2, 172 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Kiene, R. P. Production of methanethiol from dimethylsulfoniopropionate in marine surface waters. Mar. Chem. 54, 69–83 (1996).

    Article  CAS  Google Scholar 

  75. Sun, J. et al. The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol. Nat. Microbiol. 1, 16065 (2016).

    Article  CAS  PubMed  Google Scholar 

  76. 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. 11, 1376–1385 (2009).

    Article  CAS  PubMed  Google Scholar 

  77. Simó, R., Grimalt, J. O., Pedrós-Alió, C. & Albaigés, J. Occurrence and transformation of dissolved dimethyl sulfur species in stratified seawater (western Mediterranean Sea). Mar. Ecol. Progr. Ser. 127, 291–299 (1995).

    Article  Google Scholar 

  78. Kiene, R. P., Linn, L. J., González, J., Moran, M. A. & Bruton, J. A. Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine bacterioplankton. Appl. Environ. Microbiol. 65, 4549–4558 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Pinhassi, J. et al. Dimethylsulfoniopropionate turnover is linked to the composition and dynamics of the bacterioplankton assemblage during a microcosm phytoplankton bloom. Appl. Environ. Microbiol. 71, 7650–7660 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Varaljay, V. A. et al. Single-taxon field measurements of bacterial gene regulation controlling DMSP fate. ISME J. 9, 1677 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Celik, E. et al. Metabolism of 2, 3-dihydroxypropane-1-sulfonate by marine bacteria. Org. Biomol. Chem. 15, 2919–2922 (2017).

    Article  CAS  PubMed  Google Scholar 

  82. Irwin, S. V., Fisher, P., Graham, E., Malek, A. & Robidoux, A. Sulfites inhibit the growth of four species of beneficial gut bacteria at concentrations regarded as safe for food. PLOS ONE 12, e0186629 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Shapiro, R. & Gazit, A. in Protein Crosslinking (ed Friedman, M.) 633–640 (Springer, 1977).

  84. Denger, K., Smits, T. H. & Cook, A. M. L-Cysteate sulpho-lyase, a widespread pyridoxal 5′-phosphate-coupled desulphonative enzyme purified from Silicibacter pomeroyi DSS-3. Biochem. J. 394, 657–664 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Weinitschke, S., Denger, K., Cook, A. M. & Smits, T. H. The DUF81 protein TauE in Cupriavidus necator H16, a sulfite exporter in the metabolism of C2 sulfonates. Microbiology 153, 3055–3060 (2007).

    Article  CAS  PubMed  Google Scholar 

  86. Kappler, U. Bacterial sulfite-oxidizing enzymes. Biochim. Biophys. Acta-Bioenergetics 1807, 1–10 (2011).

    Article  CAS  Google Scholar 

  87. Dahl, C., Franz, B., Hensen, D., Kesselheim, A. & Zigann, R. Sulfite oxidation in the purple sulfur bacterium Allochromatium vinosum: identification of SoeABC as a major player and relevance of SoxYZ in the process. Microbiology 159, 2626–2638 (2013).

    Article  CAS  PubMed  Google Scholar 

  88. Lehmann, S. Sulfite Dehydrogenases in Organotrophic Bacteria: Enzymes, Genes and Regulation. PhD Thesis, Univ. Konstanz (2013).

  89. Meyer, B. & Kuever, J. Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5′-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes. Microbiology 153, 3478–3498 (2007).

    Article  CAS  PubMed  Google Scholar 

  90. Speciale, G., Jin, Y., Davies, G. J., Williams, S. J. & Goddard-Borger, E. D. YihQ is a sulfoquinovosidase that cleaves sulfoquinovosyl diacylglyceride sulfolipids. Nat. Chem. Biol. 12, 215 (2016).

    Article  CAS  PubMed  Google Scholar 

  91. Denger, K. et al. Sulphoglycolysis in Escherichia coli K-12 closes a gap in the biogeochemical sulphur cycle. Nature 507, 114–117 (2014). The bacterial pathway for degradation of sulfoquinovose, the sulfonate head group of sulfolipids, is discovered after many years of conjecture.

    Article  CAS  PubMed  Google Scholar 

  92. Felux, A.-K., Spiteller, D., Klebensberger, J. & Schleheck, D. Entner–Doudoroff pathway for sulfoquinovose degradation in Pseudomonas putida SQ1. Proc. Natl Acad. Sci. USA 112, E4298–E4305 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Levine, N. M. et al. Environmental, biochemical and genetic drivers of DMSP degradation and DMS production in the Sargasso Sea. Environ. Microbiol. 14, 1210–1223 (2012).

    Article  CAS  PubMed  Google Scholar 

  94. Koch, T. & Dahl, C. A novel bacterial sulfur oxidation pathway provides a new link between the cycles of organic and inorganic sulfur compounds. ISME J. 12, 2479 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Fogg, G. E. The ecological significance of extracellular products of phytoplankton photosynthesis. Bot. Marina 26, 3–14 (1983).

    Article  CAS  Google Scholar 

  96. Morán, X. A. G., Ducklow, H. W. & Erickson, M. Carbon fluxes through estuarine bacteria reflect coupling with phytoplankton. Mar. Ecol. Progr. Ser. 489, 75–85 (2013).

    Article  CAS  Google Scholar 

  97. Flynn, K. J., Clark, D. R. & Xue, Y. Modeling the release of dissolved organic matter by phytoplankton 1. J. Phycol. 44, 1171–1187 (2008).

    Article  CAS  PubMed  Google Scholar 

  98. Liss, P. S., Hatton, A. D., Malin, G., Nightingale, P. D. & Turner, S. M. Marine sulphur emissions. Philos. Trans. R. Soc. Lond. B, Biol. Sci. 352, 159–169 (1997).

    Article  CAS  Google Scholar 

  99. Seymour, J. R., Simó, R., Ahmed, T. & Stocker, R. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329, 342–345 (2010). The importance of the metabolite-enriched region surrounding phytoplankton cells for enabling interactions with bacteria is explored from physics and biological perspectives.

    Article  CAS  PubMed  Google Scholar 

  100. Strom, S., Wolfe, G., Slajer, A., Lambert, S. & Clough, J. Chemical defense in the microplankton II: inhibition of protist feeding by β-dimethylsulfoniopropionate (DMSP). Limnol. Oceanogr. 48, 230–237 (2003).

    Article  CAS  Google Scholar 

  101. Wolfe, G. V., Steinke, M. & Kirst, G. O. Grazing-activated chemical defence in a unicellular marine alga. Nature 387, 894 (1997).

    Article  CAS  Google Scholar 

  102. Obernosterer, I. & Herndl, G. J. Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N: P ratio. Mar. Ecol. Progr. Ser. 116, 247–257 (1995).

    Article  Google Scholar 

  103. Sunda, W., Kieber, D., Kiene, R. & Huntsman, S. An antioxidant function for DMSP and DMS in marine algae. Nature 418, 317–320 (2002).

    Article  CAS  PubMed  Google Scholar 

  104. Stefels, J. Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J. Sea Res. 43, 183–197 (2000).

    Article  CAS  Google Scholar 

  105. Keller, M. D. & Korjeff-Bellows, W. in Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds (eds Kiene, R. P., Visscher, P. T., Keller, M. D. & Kirst, G. O.) 131–142 (Springer, 1996).

  106. Sunda, W. G., Hardison, R., Kiene, R. P., Bucciarelli, E. & Harada, H. The effect of nitrogen limitation on cellular DMSP and DMS release in marine phytoplankton: climate feedback implications. Aquat. Sci. 69, 341–351 (2007).

    Article  CAS  Google Scholar 

  107. Durham, B. P. et al. Recognition cascade and metabolite transfer in a marine bacteria-phytoplankton model system. Environ. Microbiol. 19, 3500–3513 (2017).

    Article  CAS  PubMed  Google Scholar 

  108. Durham, B. P. et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proc. Natl Acad. Sci. USA 112, 453–457 (2015).

    Article  CAS  PubMed  Google Scholar 

  109. Seymour, J. R., Amin, S. A., Raina, J.-B. & Stocker, R. Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat. Microbiol. 2, 17065 (2017).

    Article  CAS  PubMed  Google Scholar 

  110. Suttle, C. A., Chan, A. M. & Cottrell, M. T. Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347, 467 (1990).

    Article  Google Scholar 

  111. Ma, X., Coleman, M. L. & Waldbauer, J. R. Distinct molecular signatures in dissolved organic matter produced by viral lysis of marine cyanobacteria. Environ. Microbiol. 20, 3001–3011 (2018).

    Article  CAS  PubMed  Google Scholar 

  112. Ankrah, N. Y. D. et al. Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition. ISME J. 8, 1089 (2014).

    Article  CAS  PubMed  Google Scholar 

  113. Dacey, J. W. & Wakeham, S. G. Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton. Science 233, 1314–1316 (1986).

    Article  CAS  PubMed  Google Scholar 

  114. Luo, H. & Moran, M. A. Evolutionary ecology of the marine Roseobacter clade. Microbiol. Mol. Biol. Rev. 78, 573–587 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Nowinski, B. et al. Microdiversity and temporal dynamics of marine bacterial dimethylsulfoniopropionate genes. Environ. Microbiol. 21, 1687–1701 (2019).

    Article  CAS  PubMed  Google Scholar 

  116. Liu, J. et al. Novel insights into bacterial dimethylsulfoniopropionate catabolism in the East China Sea. Front. Microbiol. 9, 3206 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  117. Reisch, C. R., Moran, M. A. & Whitman, W. B. Dimethylsulfoniopropionate-dependent demethylase (DmdA) from Pelagibacter ubique and Silicibacter pomeroyi. J. Bacteriol. 190, 8018–8024 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Sañudo-Wilhelmy, S. A., Gómez-Consarnau, L., Suffridge, C. & Webb, E. A. The role of B vitamins in marine biogeochemistry. Annu. Rev. Mar. Sci. 6, 339–367 (2014).

    Article  Google Scholar 

  119. Geng, H. & Belas, R. Expression of tropodithietic acid biosynthesis is controlled by a novel autoinducer. J. Bacteriol. 192, 4377–4387 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Steinberg, D. K. et al. Overview of the US JGOFS Bermuda atlantic time-series study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep-Sea Res. Pt II 48, 1405–1447 (2001).

    Article  CAS  Google Scholar 

  121. Karl, D. M. & Lukas, R. The Hawaii Ocean Time-Series (HOT) program: background, rationale and field implementation. Deep-Sea Res. Pt II 43, 129–156 (1996).

    Article  CAS  Google Scholar 

  122. Gorzynska, A. K., Denger, K., Cook, A. M. & Smits, T. H. Inducible transcription of genes involved in taurine uptake and dissimilation by Silicibacter pomeroyi DSS-3. Arch. Microbiol. 185, 402 (2006).

    Article  CAS  Google Scholar 

  123. Morris, R. M. et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420, 806 (2002).

    Article  CAS  PubMed  Google Scholar 

  124. Fiore, C. L., Longnecker, K., Kido Soule, M. C. & Kujawinski, E. B. Release of ecologically relevant metabolites by the cyanobacterium Synechococcus elongatus CCMP 1631. Environ. Microbiol. 17, 3949–3963 (2015).

    Article  CAS  PubMed  Google Scholar 

  125. Heal, K. R., Kellogg, N. A., Carlson, L. T., Lionheart, R. M. & Ingalls, A. E. Metabolic consequences of cobalamin scarcity in the diatom thalassiosira pseudonana as revealed through metabolomics. Protist 170, 328–348 (2019).

    Article  CAS  PubMed  Google Scholar 

  126. Boysen, A. K., Heal, K. R., Carlson, L. T. & Ingalls, A. E. Best-matched internal standard normalization in liquid chromatography–mass spectrometry metabolomics applied to environmental samples. Anal. Chem. 90, 1363–1369 (2018).

    Article  CAS  PubMed  Google Scholar 

  127. Beyersmann, P. G. et al. Dual function of tropodithietic acid as antibiotic and signaling molecule in global gene regulation of the probiotic bacterium Phaeobacter inhibens. Sci. Rep. 7, 730 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Marinov, I., Doney, S. C. & Lima, I. D. Response of ocean phytoplankton community structure to climate change over the 21st century: partitioning the effects of nutrients, temperature and light. Biogeosciences 7, 3941–3959 (2010).

    Article  Google Scholar 

  129. Taylor, G. T. et al. Ecosystem responses in the southern Caribbean Sea to global climate change. Proc. Natl Acad. Sci. USA 109, 19315–19320 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  130. Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J. & Smith, A. G. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438, 90 (2005).

    Article  CAS  PubMed  Google Scholar 

  131. Chisholm, S. W. et al. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334, 340 (1988).

    Article  Google Scholar 

  132. Waterbury, J. B., Watson, S. W., Guillard, R. R. & Brand, L. E. Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium. Nature 277, 293 (1979).

    Article  Google Scholar 

  133. Van Mooy, B. A., Rocap, G., Fredricks, H. F., Evans, C. T. & Devol, A. H. Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc. Natl Acad. Sci. USA 103, 8607–8612 (2006).

    Article  CAS  Google Scholar 

  134. Derelle, E. et al. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc. Natl Acad. Sci. USA 103, 11647–11652 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Worden, A. Z. et al. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324, 268–272 (2009).

    Article  CAS  PubMed  Google Scholar 

  136. Keller, M. D., Bellows, W. K. & Guillard, R. R. in Biogenic Sulfur in the Environment (eds Saltzman, E. S. & Cooper W. J.) 167–182 (ACS Publications, 1989).

  137. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    Article  CAS  PubMed  Google Scholar 

  138. Biller, S. J. et al. Marine microbial metagenomes sampled across space and time. Sci. Data 5, 180176 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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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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Authors and Affiliations

  1. Department of Marine Sciences, University of Georgia, Athens, GA, USA

    Mary Ann Moran

  2. School of Oceanography, University of Washington, Seattle, WA, USA

    Bryndan P. Durham

  3. Department of Biology, University of Florida, Gainesville, FL, USA

    Bryndan P. Durham

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  1. Mary Ann Moran
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  2. Bryndan P. Durham
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The authors contributed equally to all aspects of the article.

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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). https://doi.org/10.1038/s41579-019-0250-1

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