Genetics and Molecular Features of Bacterial Dimethylsulfoniopropionate (DMSP) and Dimethyl Sulfide (DMS) Transformations

  • J. M. GonzálezEmail author
  • A. W. B. Johnston
  • M. Vila-Costa
  • A. Buchan
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


The transformations of dimethylsulfoniopropionate (DMSP; (CH3)2S+CH2CH2COO) by bacterioplankton play important roles in the global sulfur cycle. This compound is produced in large quantities primarily for use as an osmolyte by marine algae. DMSP is a labile compound although the complete mineralization of DMSP is only a minor fate in the ocean. DMSP is the main precursor of dimethyl sulfide (DMS; CH3–S–CH3), a radiatively active trace gas that contributes to global climate regulation. However, it is believed that the main pathway for the transformation of DMSP involves an assimilation step in which DMSP sulfur is incorporated efficiently into cell biomass, leaving relatively little sulfur available for release as DMS. DMSP is rapidly turned over in the environment and the diversity of pathways for its transformation are likely not yet fully realized. This chapter covers recent findings on the genetics of DMSP catabolism; their discoveries are changing our view of the role of this compound in the world’s oceans. Although even less is known about bacterially mediated transformations of DMS, the handful of genes that have been described in a limited number of bacteria is also reviewed in this chapter.


  1. Baxter NJ, Scanlan J, De Marco P, Wood AP, Murrell JC (2002) Duplicate copies of genes encoding methanesulfonate monooxygenase in Marinosulfonomonas methylotropha strain TR3 and detection of methanesulfonate utilizers in the environment. Appl Environ Microbiol 68:289–296CrossRefPubMedPubMedCentralGoogle Scholar
  2. Borodina E, Kelly DP, Rainey FA, Ward-Rainey NL, Wood AP (2000) Dimethylsulfone as a growth substrate for novel methylotrophic species of Hyphomicrobium and Arthrobacter. Arch Microbiol 173:425–437CrossRefPubMedGoogle Scholar
  3. Bürgmann H, Howard EC, Ye W, Sun F, Sun S, Napierala S, Moran MA (2007) Transcriptional response of Silicibacter pomeroyi DSS-3 to dimethylsulfoniopropionate (DMSP). Environ Microbiol 9:2742–2755CrossRefPubMedGoogle Scholar
  4. Charlson RJ, Lovelock JE, Andreae MO, Warren SG (1987) Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326:655–661CrossRefGoogle Scholar
  5. Cosquer A, Pichereau V, Pocard J-A, Minet J, Cormier M, Bernard T (1999) Nanomolar levels of dimethylsulfoniopropionate, dimethylsulfonioacetate, and glycine betaine are sufficient to confer osmoprotection to Escherichia coli. Appl Environ Microbiol 65:3304–3311PubMedPubMedCentralGoogle Scholar
  6. Curson AR, Rogers R, Todd JD, Brearley CA, Johnston AW (2008) Molecular genetic analysis of a dimethylsulfoniopropionate lyase that liberates the climate-changing gas dimethylsulfide in several marine α-proteobacteria and Rhodobacter sphaeroides. Environ Microbiol 10:757–767CrossRefPubMedGoogle Scholar
  7. De Bont JAM, van Dijken JP, Harder W (1981) Dimethyl sulphoxide and dimethyl sulphide as a carbon, sulphur and energy source for growth of Hyphomicrobium S. J Gen Microbiol 127:315–323Google Scholar
  8. De Marco P, Moradas-Ferreira P, Higgins TP, McDonald I, Kenna EM, Murrell JC (1999) Molecular analysis of a novel methanesulfonic acid monooxygenase from the methylotroph Methylosulfonomonas methylovora. J Bacteriol 181:2244–2251PubMedPubMedCentralGoogle Scholar
  9. De Souza MP, Yoch DC (1996) N-terminal amino acid sequences and comparison of DMSP lyases from Pseudomonas doudoroffii and Alcaligenes strain M3A. In: Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Environmental and biological chemistry on dimethylsulfoniopropionate and related sulfonium compounds. Plenum Press, New York, pp 293–304CrossRefGoogle Scholar
  10. Del Valle DA, Kieber DJ, Kiene RP (2007) Depth-dependent fate of biologically-consumed dimethylsulfide in the Sargasso Sea. Mar Chem 103:197–208CrossRefGoogle Scholar
  11. DeZwart JMM, Nelisse PN, Kuenen JG (1996) Isolation and characterization of Methylophaga sulfidovorans sp. nov.: an obligately methylotrophic, aerobic, dimethylsulfide oxidizing bacterium from a microbial mat. FEMS Microbiol Ecol 20:261–270CrossRefGoogle Scholar
  12. Endoh T, Kasuga K, Horinouchi M, Yoshida T, Habe H, Nojiri H, Omori T (2003) Characterization and identification of genes essential for dimethyl sulfide utilization in Pseudomonas putida strain DS1. Appl Microbiol Biotechnol 62:83–91CrossRefPubMedGoogle Scholar
  13. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67:2873–2882CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fuse H, Takimura O, Murakami K, Yamaoka Y, Omori T (2000) Utilization of dimethyl sulfide as a sulfur source with the aid of light by Marinobacterium sp. strain DMS-S1. Appl Environ Microbiol 66:5527–5532CrossRefPubMedPubMedCentralGoogle Scholar
  15. González JM, Kiene RP, Moran MA (1999) Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class Proteobacteria. Appl Environ Microbiol 65:3810–3819PubMedPubMedCentralGoogle Scholar
  16. Hanlon SP, Holt RA, Moore GR, McEwan AG (1994) Isolation and characterization of a strain of Rhodobacter sulfidophilus: a bacterium which grows autotrophically with dimethylsulfide as electron-donor. Microbiology 140:1953–1958CrossRefGoogle Scholar
  17. Horinouchi M, Kasuga K, Nojiri H, Yamane H, Omori T (1997) Cloning and characterization of genes encoding an enzyme which oxidizes dimethyl sulfide in Acinetobacter sp. strain 20B. FEMS Microbiol Lett 155:99–105CrossRefPubMedGoogle Scholar
  18. Howard EC, Henriksen JR, Buchan A, Reisch CR, Bürgmann H, Welsh R, Ye W, González JM, Mace K, Joye SB, Kiene RP, Whitman WB, Moran MA (2006) Bacterial taxa that limit sulfur flux from the ocean. Science 314:649–652CrossRefPubMedGoogle Scholar
  19. Howard EC, Sun S, Biers EJ, Moran MA (2008) Abundant and diverse bacteria involved in DMSP degradation in marine surface waters. Environ Microbiol 10:2397–2410CrossRefPubMedGoogle Scholar
  20. Kanagawa T, Kelly DP (1986) Breakdown of dimethyl sulfide by mixed cultures and by Thiobacillus thioparus. FEMS Microbiol Lett 34:13–19CrossRefGoogle Scholar
  21. Kettle AJ, Andreae MO (2000) Flux of dimethylsulfide from the oceans: a comparison of updated data sets and flux models. J Geophys Res 26:26793–26808CrossRefGoogle Scholar
  22. Kiene RP, Linn LJ (2000) Distribution and turnover of dissolved DMSP and its relationships with bacterial production and dimethylsulfide in the Gulf of Mexico. Limnol Oceanogr 45:849–861CrossRefGoogle Scholar
  23. Kiene RP, Oremland RS, Catena A, Miller LG, Capone DG (1986) Metabolism of reduced methylated sulfur compounds in anaerobic sediments and by a pure culture of an estuarine methanogen. Appl Environ Microbiol 52:1037–1045PubMedPubMedCentralGoogle Scholar
  24. Kiene RP, Hoffman Williams LP, Walker JE (1998) Seawater microorganisms have a high affinity glycine betaine uptake system which also recognizes dimethylsulfoniopropionate. Aquat Microb Ecol 15:39–51CrossRefGoogle Scholar
  25. Kiene RP, Linn LJ, González JM, Moran MA, Bruton JA (1999) Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine bacterioplankton. Appl Environ Microbiol 65:4549–4558PubMedPubMedCentralGoogle Scholar
  26. Kiene RP, Linn LJ, Bruton JA (2000) New and important roles for DMSP in marine microbial communities. J Sea Res 43:209–224CrossRefGoogle Scholar
  27. Malmstrom RR, Kiene RP, Cottrell MT, Kirchman DL (2004) Contribution of SAR11 bacteria to dissolved dimethylsulfoniopropionate and amino acid uptake in the North Atlantic ocean. Appl Environ Microbiol 70:4129–4135CrossRefPubMedPubMedCentralGoogle Scholar
  28. Moran MA, Buchan A, González JM, Heidelberg JF, Whitman WB, Kiene RP et al (2004) Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432:910–913CrossRefPubMedGoogle Scholar
  29. Moran MA, Belas R, Schell MA, González JM, Sun F, Sun S et al (2007) Ecological genomics of marine roseobacters. Appl Environ Microbiol 73:4559–4569CrossRefPubMedPubMedCentralGoogle Scholar
  30. Omori T, Saiki Y, Kasuga K, Kodama T (1995) Desulfurization of alkyl and aromatic sulfides and sulfonates by dibenzothiophene-desulfurizing Rhodococcus sp. strain SY1. Biosci Biotechnol Biochem 59:1195–1198CrossRefGoogle Scholar
  31. Pol A, Op den Camp HJ, Mees SG, Kersten MA, van der Drift C (1994) Isolation of a dimethylsulfide-utilizing Hyphomicrobium species and its application in biofiltration of polluted air. Biodegradation 5:105–112CrossRefPubMedGoogle Scholar
  32. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S et al (2007) Oceanic metagenomics: the Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e77CrossRefPubMedPubMedCentralGoogle Scholar
  33. Schaefer JF, Goodwin KD, McDonald IR, Murrell JC, Oremland RS (2002) Leisingera methylohalidivorans gen. nov., sp. nov., a marine methylotroph that grows on methyl bromide. Int J Syst Evol Microbiol 52:851–859PubMedGoogle Scholar
  34. Schäfer H (2007) Isolation of Methylophaga spp. from marine dimethylsulfide-degrading enrichment cultures and identification of polypeptides induced during growth on dimethylsulfide. Appl Environ Microbiol 73:2580–2591CrossRefPubMedPubMedCentralGoogle Scholar
  35. Simó R (2001) Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends Ecol Evol 16:287–294CrossRefPubMedGoogle Scholar
  36. Simó R, Pedrós-Alió C (1999) Short-term variability in the open ocean cycle of dimethylsulfide. Global Biogeochem Cycles 13:1173–1181CrossRefGoogle Scholar
  37. Simó R, Archer SD, Pedrós-Alió C, Gilpin L, Stelfox-Widdicombe CE (2002) Coupled dynamics of dimethylsulfoniopropionate and dimethylsulfide cycling and the microbial food web in surface waters of the North Atlantic. Limnol Oceanogr 47:53–61CrossRefGoogle Scholar
  38. Suylen GMH, Kuenen JG (1986) Chemostat enrichment and isolation of Hyphomicrobium EG a dimethyl sulfide oxidizing methylotroph and reevaluation of Thiobacillus MS1. Antonie Leeuwenhoek 52:281–293CrossRefPubMedGoogle Scholar
  39. Suylen GMH, Stefess GC, Kuenen JG (1986) Chemolithotrophic potential of a Hyphomicrobium species, capable of growth on methylated sulphur compounds. Arch Microbiol 146:192–198CrossRefGoogle Scholar
  40. Suylen GMH, Large PJ, van Dijken JP, Kuenen JG (1987) Methyl mercaptan oxidase, a key enzyme in the metabolism of methylated sulphur compounds by Hyphomicrobium EG. J Gen Microbiol 133:2989–2997Google Scholar
  41. Tanimoto Y, Bak F (1994) Anaerobic degradation of methylmercaptan and dimethyl sulfide by newly isolated thermophilic sulfate-reducing bacteria. Appl Environ Microbiol 60:2450–2455PubMedPubMedCentralGoogle Scholar
  42. Todd JD, Rogers R, Li YG, Wexler M, Bond PL, Sun L, Curson AR, Malin G, Steinke M, Johnston AW (2007) Structural and regulatory genes required to make the gas dimethyl sulfide in bacteria. Science 315:666–669CrossRefPubMedGoogle Scholar
  43. Tripp JH, Kitner JB, Schwalbach MS, Dacey JWH, Wilhelm LJ, Giovannoni SJ (2008) SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452:741–744CrossRefPubMedGoogle Scholar
  44. Vallino JJ, Hopkinson CS, Hobbie JE (1996) Modeling bacterial utilization of dissolved organic matter: optimization replaces Monod growth kinetics. Limnol Oceanogr 41:1591–1609CrossRefGoogle Scholar
  45. Vila M, Simó R, Kiene RP, Pinhassi J, González JM, Moran MA, Pedrós-Alió C (2004) Use of microautoradiography combined with fluorescence in situ hybridization to determine dimethylsulfoniopropionate incorporation by marine bacterioplankton taxa. Appl Environ Microbiol 70:4648–4657CrossRefPubMedPubMedCentralGoogle Scholar
  46. Vila-Costa M, del Valle DA, González JM, Slezak D, Kiene RP, Sánchez O, Simó R (2006) Phylogenetic identification and metabolism of marine dimethylsulfide-consuming bacteria. Environ Microbiol 8:2189–2200CrossRefPubMedGoogle Scholar
  47. Vila-Costa M, Pinhassi J, Alonso C, Pernthaler J, Simó R (2007) An annual cycle of dimethylsulfoniopropionate-sulfur and leucine assimilating bacterioplankton in the coastal NW Mediterranean. Environ Microbiol 9:2451–2463CrossRefPubMedGoogle Scholar
  48. Visscher PT, Taylor BF (1994) Demethylation of dimethylsulfoniopropionate to 3-mercaptopropionate by an aerobic marine bacterium. Appl Environ Microbiol 60:4617–4619PubMedPubMedCentralGoogle Scholar
  49. Yoch DC (2002) Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl Environ Microbiol 68:5804–5815CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • J. M. González
    • 1
    Email author
  • A. W. B. Johnston
    • 2
  • M. Vila-Costa
    • 3
  • A. Buchan
    • 4
    • 5
  1. 1.Department of MicrobiologyUniversity of La LagunaTenerifeSpain
  2. 2.School of Biological SciencesUniversity of East AngliaNorwichUK
  3. 3.Department of Marine SciencesUniversity of GeorgiaAthensUSA
  4. 4.Department of Continental Ecology-LimnologyCentre d’Estudis Avançats de Blanes, CSICBlanesSpain
  5. 5.Department of MicrobiologyUniversity of TennesseeKnoxvilleUSA

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