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Aerobic Bacterial Catabolism of Dimethylsulfoniopropionate

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Aerobic Utilization of Hydrocarbons, Oils, and Lipids

Part of the book series: Handbook of Hydrocarbon and Lipid Microbiology ((HHLM))

Abstract

Dimethylsulfoniopropionate (DMSP) is an organosulfur zwitterion produced by various marine algae and Bacteria as an osmolyte, cryoprotectant, defense molecule, and antioxidant. In the marine environment in particular, it can be degraded by the Bacteria in various ways. In this chapter we cover the biochemistry and physiology of the various pathways of DMSP catabolism, including the three core enzymes DMSP dethiomethylase (EC 4.4.1.3, the so-called DMSP lyase), DMSP demethylase (EC 2.1.1.269), and DMSP CoA transferase/lyase (EC 2.3.1.x). Six isoenzyme classes of DMSP dethiomethylase have been purified and confirmed in marine Bacteria thus far, with a further isoenzyme found in algae that may also occur in Bacteria – these are all discussed in detail. Methodologies for enzyme assays and the synthesis of DMSP hydrochloride are given, including those for radio- and stable-isotope labelling.

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References

  • Alcolombri U, Elias M, Vardi A, Tawfik DS (2014a) Ambiguous evidence for assigning DddQ as a dimethylsulfoniopropionate lyase and oceanic dimethylsulfide producer. Proc Natl Acad Sci 111:E2078–E2079

    Article  CAS  Google Scholar 

  • Alcolombri U, Laurino P, Lara-Astiaso P, Vardi A, Tawfik DS (2014b) DddD is a co-A-transferase/lyase producing dimethyl sulfide in the marine environment. Biochemistry 53:5473–5475

    Article  CAS  Google Scholar 

  • Alcolombri U, Ben-Dor S, Feldmesser E, Levin Y, Tawfik DS, Vardi A (2015) Identification of the algal dimethyl sulfide-releasing enzyme: a missing link in the marine sulfur cycle. Science 348:1466–1469

    Article  CAS  Google Scholar 

  • Alcolombri U, Lei L, Meltzer D, Vardi A, Tawfik DS (2017) Assigning the algal source of dimethylsulfide using a selective lyase inhibitor. ACS Chem Biol 12:41–46

    Article  CAS  Google Scholar 

  • Arnáiz FJ (1995) A convenient way to generate hydrogen chloride in the freshman lab. J Chem Educ 72:1139

    Article  Google Scholar 

  • Aronoff S (1956) Techniques of radiobiochemistry. Iowa State College Press, Ames

    Google Scholar 

  • Bazan JF, Weaver LH, Roderick SL, Huber R, Matthews BW (1994) Sequence and structure comparison suggest that methionine aminopeptidase, prolidase, aminopeptidase p, and creatinase share a common fold. Proc Natl Acad Sci 91:2473–2477

    Article  CAS  Google Scholar 

  • Bobbio FO, Bobbio PA, de Souza SC (1987) Separation and identification of cinnamic acids by TLC. J Chem Educ 64:182–182

    Article  CAS  Google Scholar 

  • Boden R, Hutt LP (2018a) Bacterial metabolism of C1 organosulfur compounds. In: Rojo F (ed) aerobic utilization of hydrocarbons, oils and lipids. Handbook of hydrocarbon and lipid metabolism. Springer, Cham

    Google Scholar 

  • Boden R, Hutt LP (2018b) Determination of kinetic parameters and metabolic modes using the chemostat. In: Steffan R (ed) Consequences of microbial interaction with hydrocarbons, oils and lipids: biodegradation and bioremediation. Handbook of hydrocarbon and lipid microbiology. Springer, Cham

    Google Scholar 

  • Brummett AE, Schincker NJ, Crider A, Todd JD, Dey M (2015) Biochemical, kinetic and spectroscopic characterization of Ruegeria pomeroyi DddW – a mononuclear iron-dependent DMSP lyase. PLoS One 10:e0127288

    Article  Google Scholar 

  • Brummett AE, Dey M (2016) New mechanistic insight from substrate- and product-bound structures of the metal-dependent dimethylsulfoniopropionate lyase DddQ. Biochemistry 55:6162–6174

    Article  CAS  Google Scholar 

  • Buchan A, Collier LS, Neidle EL, Moran MA (2000) Key aromatic-ring-cleaving enzyme, protocatechuate 3,4-dioxygenase, in the ecologically important Roseobacter lineage. Appl Environ Microbiol 66:4662–4672

    Article  CAS  Google Scholar 

  • Bullock HA, Luo H, Whitman WB (2017) Evolution of dimethylsulfoniopropionate metabolism in marine phytoplankton and bacteria. Front Microbiol 8:637

    PubMed  PubMed Central  Google Scholar 

  • Burkhardt I, Lauterbach L, Brock NL, Dickschat JS (2017) Chemical differentiation of three DMSP lyases from the marine Roseobacter group. Org Biomol Chem 15:4432–4439

    Article  CAS  Google Scholar 

  • Cao HY, Wang P, Xu F, Li PY, Xie BB, Qin QL, Zhang YZ, Li CY, Chen XL (2017) Molecular insight into the acryloyl-CoA hydration by AcuH for acrylate detoxification in dimethylsulfoniopropionate-catabolizing bacteria. Front Microbiol 8:2034

    Article  Google Scholar 

  • Challenger F, Simpson MI (1948) Studies on biological methylation. Part XII. A precursor of dimethyl sulfide evolved by Polysyphonia fastigiata.Dimethyl-2-carboxyethylsulfonium hydroxide and its salts. J Chem Soc 0:1591–1597

    Article  CAS  Google Scholar 

  • Charlson RJ, Lovelock JE, Andreae MO, Warren SG (1987) Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326:655–661.

    Article  CAS  Google Scholar 

  • 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 10:757–767

    Article  CAS  Google Scholar 

  • Curson AR, Sullivan MK, Todd JD, Johnston AW (2010) Identification of genes for dimethyl sulfide production in bacteria in the gut of Atlantic herring (Culpea hargengus). ISME J 4:144–146

    Article  Google Scholar 

  • Curson AR, Sullivan MJ, Todd JD, Johnston AW (2011) DddY, a periplasmic dimethylsulfoniopropionate lyase found in taxonomically diverse species of Proteobacteria. ISME J 5:1191–1200

    Article  CAS  Google Scholar 

  • Curson ARJ, Liu J, Bermejo Martínez A, Green RT, Chan Y, Carrión O, Williams BT, Zhang S-H, Yang G-P, Bulman Page PC, Zhang X-H, Todd JD (2017) Dimethylsulfoniopropionate biosynthesis in marine bacteria and identification of the key gene in this process. Nat Microbiol 2:17009

    Article  CAS  Google Scholar 

  • del Valle DA, Slezak D, Smith CM, Rellinger AN, Kieber DJ, Kiene RP (2011) Effect of acidification on preservation of DMSP in seawater and phytoplankton cultures: evidence for rapid loss and cleavage of DMSP in samples containing Phaeocystis sp. Mar Chem 124:57–67

    Article  Google Scholar 

  • Erb TJ, Fuchs G, Alber BE (2009) (2S)-methylsuccinyl-CoA dehydrogenase closes the ethylmalonyl-CoA pathway for acetyl-CoA assimilation. Mol Microbiol 73:922–1008

    Article  Google Scholar 

  • Fowler EK (2015) On the molecular diversity of dimethylsulphoniopropionate catabolism by marine bacteria. Ph.D Thesis. University of East Anglia, UK

    Google Scholar 

  • Haas P (1935) The liberation of methyl sulphide by seaweed. Biochem J 29:1297–1299

    Article  CAS  Google Scholar 

  • Heck RF, Nolley JP (1972) Palladium-catalyzed vinylic hydrogen substitution reactions with aryl, benzyl and styryl halides. J Org Chem 37:2320–2322

    Article  CAS  Google Scholar 

  • Hehemann J-H, Law A, Redecke L, Boraston AB (2014) The structure of RdDddP from Roseobacter denitrificans reveals that DMSP lyases in the DddP-family are metalloenzymes. PLoS One 9:e103128

    Article  Google Scholar 

  • Keine RP (1993) Microbial sources and sinks for methylated sulfur compounds in the marine environment. In: Murrell JC, Kelly DP (eds) Microbial growth on C1 compounds. Intercept Ltd, Andover, pp 15–34

    Google Scholar 

  • Keine RP (1996) Microbiological controls on dimethylsulfide emissions from wetlands and the ocean. In: Murrell JC, Kelly DP (eds) NATO ASI series vol 39. Microbiology of atmospheric trace gases. Springer-Verlag, Berlin, pp 205–225

    Chapter  Google Scholar 

  • Keine RP, Taylor BF (1988) Biotransformations of organosulfur compounds in sediments via 3-mercaptopropionate. Nature 322:148–150

    Article  Google Scholar 

  • Kelly DP (1996) A global perspective on sources and sinks of biogenic trace gases: an atmospheric system driven by microbiology. In: Murrell JC, Kelly DP (eds) NATO ASI series vol 39. Microbiology of atmospheric trace gases. Springer-Verlag, Berlin, pp 1–16

    Google Scholar 

  • Kelly DP, Malin G, Wood AP (1993) Microbial transformations and biogeochemical cycling of one-carbon substrates containing sulphur, nitrogen or halogens. In: Murrell JC, Kelly DP (eds) Microbial growth on C1 compounds. Intercept Ltd, Andover, pp 47–63

    Google Scholar 

  • Kinsey JD, Kieber DJ (2016) Microwave preservation method for DMSP, DMSO, and acrylate in unfiltered seawater and phytoplankton culture samples. Limnol Oceanogr Methods 14:196–209

    Article  CAS  Google Scholar 

  • Kirkwood M, Le Brun NE, Todd JD, Johnston AWB (2010) ThedddP gene of Roseovarius nubinhibens encodes a novel lyase that cleaves dimethylsulfoniopropionate into acrylate plus dimethyl sulfide. Microbiology (UK) 156:1900–1906

    Article  CAS  Google Scholar 

  • Lei L, Phaneendra Cherukuri K, Alcolombri U, Meltzer D, Tawfik DS (2018) The dimethylsulfoniopropionate (DMSP) lyase and lyase-like cupin family consists of bona fide DMSP lyases as well as other enzymes with unknown function. Biochemistry 57:3364–3377

    Article  CAS  Google Scholar 

  • Leys D, Brasan J, Scrutton NS (2003) Channelling and formation of ‘active’ formaldehyde in dimethylglycine oxidase. EMBO J 22:4038–4048

    Article  CAS  Google Scholar 

  • Li TD, Doronina NV, Ivanova EG, IuA T (2007) Vitamin B12-independent strains of Methylophaga marina isolated from Red Sea algae. Mikrobiologiia 76:88–94

    PubMed  Google Scholar 

  • Li C-Y, Wei T-D, Zhang S-H, Chen X-L, Gao X, Wang P, Xie B-B, Su H-N, Qin Q-L, Zhang X-Y, Yu J, Zhang H-H, Zhou B-C, Yang G-P, Zhang Y-Z (2014a) Molecular insight into bacterial cleavage of oceanic dimethylsulfoniopropionate into dimethyl sulfide. Proc Natl Acad Sci 111:1026–1031

    Article  CAS  Google Scholar 

  • Li C-Y, Chen X-L, Xie B-B, Su H-N, Qin Q-L, Zhang Y-Z (2014b) Reply to Tawfik et al.: DddQ is a dimethylsulfoniopropionate lyase involved in dimethylsulfoniopropionate catabolism in marine bacterial cells. Proc Natl Acad Sci 111:E2080

    Article  CAS  Google Scholar 

  • Li C-Y, Zhang D, Chen X-L, Wang P, Shi W-L, Li P-L, Zhang X-Y, Qin Q-L, Todd JD, Zhang Y-Z (2017) Mechanistic insights into dimethylsulfoniopropionate lyase DddY, a new member of the cupin superfamily. J Mol Biol 429:3850–3862

    Article  CAS  Google Scholar 

  • Mei S, Taejun C, Tetsuya T, Hitomi O, Yuji A (2015) A simple TLC-densitometric method for the quantification of acrylic acid in aqueous solutions. J Plan Chromatgr Mod TLC 28:12–16

    Article  Google Scholar 

  • Michael A (1886) Ueber die Addition von Natriumacetissig- und Natriummalonsäureäthern zu den Aethern ungesättigter Säuren. J Prakt Chem 35:349–356

    Article  Google Scholar 

  • Otte ML, Wilson G, Morris JT, Moran BM (2004) Dimethylsulfoniopropionate (DMSP) and related compounds in higher plants. J Exp Bot 55:1919–1925

    Article  CAS  Google Scholar 

  • Przyjazny A, Janicki W, Chrzanowski W, Staszewski R (1983) Headspace gas chromatographic determinations of distribution coefficients of selected organosulphur compounds and their dependence on some parameters. J Chromatogr 280:249–260

    Article  CAS  Google Scholar 

  • Raina JB, Tapiolas D, Willis BL, Bourne DG (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 75:3492–3501

    Article  CAS  Google Scholar 

  • Reisch CR, Moran MA, Whitman WB (2008) Dimethylsulfoniopropionate-dependent demethylase (DmdA) from Pelagibacter ubique and Silicibacter pomeroyi. J Bacteriol 190:8018–8024

    Article  CAS  Google Scholar 

  • Reisch CR, Moran MA, Whitman WB (2011a) Bacterial catabolism of dimethylsulfoniopropionate (DMSP). Front Microbiol 2:172

    Article  CAS  Google Scholar 

  • Reisch CR, Stoudemayer MJ, Varaljay VA, Amster IJ, Moran MA, Whitman WB (2011b) Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria. Nature 473:208–211

    Article  CAS  Google Scholar 

  • Reisch CR, Crabb WM, Gifford SM, Teng Q, Stoudemayer MJ, Moran MA, Whitman WB (2013) Metabolism of dimethylsulfoniopropionate by Ruegeria pomeroyi DSS-3. Mol Microbiol 89:774–791

    Article  CAS  Google Scholar 

  • Schäfer H, Myronova N, Boden R (2010) Microbial degradation of dimethylsulphide and related C1-Sulphur compounds: organisms and pathways controlling fluxes of Sulphur in the biosphere. J Exp Bot 61:315–334

    Article  Google Scholar 

  • Schnicker NJ, de Silva SM, Todd JD, Dey M (2017) Structural and biochemical insights into dimethylsulfoniopropionate cleavage by cofactor-bound DddK from the prolific marine bacterium Pelagibacter. Biochemistry 56:2873–2885

    Article  CAS  Google Scholar 

  • Schuller DK, Reisch CR, Moran MA, Whitman WB, Lanzilotta WN (2012) Structures of dimethylsulfoniopropionate-dependent demethylase from the marine organism Pelagabacter ubique. Protein Sci 21:289–298

    Article  CAS  Google Scholar 

  • Scrutton NS, Leys D (2005) Crystal structure of DMGO provides a prototype for a new tetrahydrofolate-binding fold. Biochem Soc Trans 33:776–779

    Article  CAS  Google Scholar 

  • Shintani H (1995) HPLC analysis of toxic additives and residual monomer from dental plate. J Liq Chromatogr 18:613–626

    Article  CAS  Google Scholar 

  • Shivani Y, Subhash Y, Ch S, ChV R (2016) Halodesulfovibrio spirochaetisodalis gen. nov., sp. nov. and reclassification of four Desulfovibrio spp. Int J Syst Evol Microbiol 67:87–93

    Google Scholar 

  • Steinke M, Wolfe GV, Kirst GO (1998) Partial characterisation of dimethylsulfoniopropionate (DMSP) lyase isozymes in 6 strains of Emiliania huxleyi. Mar Ecol Prog Ser 175:215–225

    Article  CAS  Google Scholar 

  • Sun J, Todd JD, Thrash JC, Qian Y, Qian MC, Temperton B, Guo J, Fowler EK, Aldrich JT, Nicora CD, Lipton MS, Smith RD, De Leenheer P, Payne SH, Johnston AW, Davie-Martin CL, Halsey KH, Giovannoni SJ (2016) The abundant marine bacterium Pelagibacter symultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol. Nat Microbiol 1:16065

    Article  CAS  Google Scholar 

  • Todd JD, Rogers R, Li YG, Wexler M, Bond PL, Sun L, Curson ARJ, Malin G, Steinke M, Johnston AWB (2007) Structural and regulatory genes required to make the gas dimethyl sulfide in bacteria. Science 315:666–669

    Article  CAS  Google Scholar 

  • Todd JD, Curson AR, Dupont CL, Nicholson P, Johnston AW (2009) 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

    Article  CAS  Google Scholar 

  • Todd JD, Curson ARJ, Kirkwood M, Sullivan MJ, Green RT, Johnston AWB (2011) DddQ, a novel, cupin-containing dimethylsulfoniopropionate lyase in marine roseobacters and in uncultured marine bacteria. Environ Microbiol 13:427–438

    Article  CAS  Google Scholar 

  • Todd JD, Kirkwood M, Newton-Payne S, Johnston AW (2012) DddW, a third DMSP lyase in a model Roseobacter marine bacterium, Ruegeria pomeroyi DSS-3. ISME J 6:223–226

    Article  CAS  Google Scholar 

  • Tripp HJ, Kitner JB, Schwalbach MS, Dacey JW, Wilhelm LJ, Giovannoni SJ (2008) SAR11 marine bacteria require exogenous reduced Sulphur for growth. Nature 452:741–744

    Article  CAS  Google Scholar 

  • van der Maarel MJEC, Aukema W, Hansen TA (1996a) Purification and characterization of a dimethylsulfoniopropionate cleaving enzyme from Desulfovibrio acrylicus. FEMS Microbiol Lett 143:3241–3245

    Google Scholar 

  • van der Maarel MJEC, van Bergeijk S, van Werkhoven AF, Laverman AM, Meijer WG, Stam WT, Hansen TA (1996b) Cleavage of dimethylsulfoniopropionate and reduction of acrylate by Desulfovibrio acrylicus sp. Arch Microbiol 166:109–115

    Article  Google Scholar 

  • Visscher PT, Taylor BF (1994) Demethylation of dimethylsulfoniopropionate to 3-mercaptopropionate by an aerobic marine bacterium. Appl Environ Microbiol 60:4617–4619

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang P, Chen X-L, Li C-Y, Gao X, Zhu D-Y, Xie B-B, Qin Q-L, Zhang X-Y, Su H-N, Zhou B-C, Xun L-Y, Zhang Y-Z (2015) Structural and molecular basis for the novel catalytic mechanism and evolution of DddP, an abundant peptidase-like bacterial dimethylsulfoniopropionate lyase: a new enzyme from an old fold. Mol Microbiol 98:289–301

    Article  CAS  Google Scholar 

  • Wang P, Cao HY, Chen XL, Li CY, Zhang XY, Qin QL, Todd JD, Zhang YZ (2017) Mechanistic insight into acrylate metabolism and detoxification in marine dimethylsulfoniopropionate-catabolizing bacteria. Mol Microbiol 105:674–688

    Article  CAS  Google Scholar 

  • White WR, Leenheer JA (1975) Determination of free formic and acetic acids by gas chromatography using the flame ionization detector. J Chromatogr Sci 13:386–389

    Article  CAS  Google Scholar 

  • Wood AP (1996) Sulfur, carbon and nitrogen interactions. In: Murrell JC, Kelly DP (eds) NATO ASI series Vol. 39. Microbiology of atmospheric trace gases. Springer-Verlag, Berlin, pp 281–295

    Google Scholar 

  • Zeng Y-X, Qiao Z-Y, Yu Y, Li H-R, Luo W (2016) Diversity of bacterial dimethylsulfoniopropionate degradation genes in surface seawater of the. Arctic Kongsfjorden Sci Rep 6:33031

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. School of Biological and Marine Sciences, Sustainable Earth Institute, Faculty of Science and Engineering, University of Plymouth, Plymouth, UK

    Rich Boden

  2. School of Biological and Marine Sciences, Faculty of Science and Engineering, University of Plymouth, Plymouth, UK

    Lee P. Hutt

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  1. Rich Boden
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  2. Lee P. Hutt
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Correspondence to Rich Boden .

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  1. Centro Nacional de Biotecnología, CSIC, Madrid, Spain

    Fernando Rojo

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Boden, R., Hutt, L.P. (2019). Aerobic Bacterial Catabolism of Dimethylsulfoniopropionate. In: Rojo, F. (eds) Aerobic Utilization of Hydrocarbons, Oils, and Lipids. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-50418-6_52

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