Skip to main content
SpringerLink
Log in

Dissimilation of C3-sulfonates

  • Mini-Review
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Cysteate and sulfolactate are widespread natural products in the environment, while propanesulfonate, 3-aminopropanesulfonate and propane-1,3-disulfonate are xenobiotics. While some understanding of the bacterial assimilation of cysteate sulfur has been achieved, details of the dissimilation of cysteate and sulfolactate by microbes together with information on the degradation of the xenobiotics have only recently become available. This minireview centres on bacterial catabolism of the carbon moiety in these C3-sulfonates and on the fate of the sulfonate group. Three mechanisms of desulfonation have been established. Firstly, cysteate is converted via sulfopyruvate to sulfolactate, which is desulfonated to pyruvate and sulfite; the latter is oxidized to sulfate by a sulfite dehydrogenase and excreted as sulfate in Paracoccus pantotrophus NKNCYSA. Secondly, sulfolactate can be converted to cysteate, which is cleaved in a pyridoxal 5′-phosphate-coupled reaction to pyruvate, sulfite and ammonium ions; in Silicibacter pomeroyi DSS-3, the sulfite is excreted largely as sulfite. Both desulfonation reactions seem to be widespread. The third desulfonation mechanism is oxygenolysis of, e.g. propanesulfonate(s), about which less is known.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson R, Kates M, Volcani BE (1979) Studies on the biosynthesis of sulfolipids in the diatom Nitzschia alba. Biochim Biophys Acta 573:557-561

    PubMed  CAS  Google Scholar 

  • Bagley PJ, Hirschberger LL, Stipanuk MH (1995) Evaluation and modification of an assay procedure for cysteine dioxygenase activity: high-performance liquid chromatography method for measurement of cysteine sulfinate and demonstration of physiological relevance of cysteine dioxygenase activity in cysteine catabolism. Anal Biochem 227:40–48

    Article  PubMed  CAS  Google Scholar 

  • 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 68:289–296

    Article  PubMed  CAS  Google Scholar 

  • Bonsen PPM, Spudich JA, Nelson DL, Kornberg A (1969) Biochemical studies of bacterial sporulation and germination XII. A sulfonic acid as a major sulfur compound of Bacillus subtilis spores. J Bacteriol 98:62–68

    PubMed  CAS  Google Scholar 

  • Booth IR, Edwards MD, Murray E, Miller S (2005) The role of bacterial channels in cell physiology. In: Kubalski A, Martinac B (eds) Bacterial ion channels and their eukaryotic homologs. ASM Press, Washington DC, pp 291–312

    Google Scholar 

  • Consden R, Gordon AH, Martin AJP (1946) The identification of amino-acids derived from cysteine in chemically modified wool. Biochem J 40:580–582

    PubMed  CAS  Google Scholar 

  • Cook AM, Denger K (2002) Dissimilation of the C2 sulfonates. Arch Microbiol 179:1–6

    Article  PubMed  CAS  Google Scholar 

  • Cook AM, Denger K (2005) Metabolism of taurine in microorganisms: a primer in molecular diversity? Adv Exp Med Biol (in press)

  • Cook AM, Laue H, Junker F (1999) Microbial desulfonation. FEMS Microbiol Rev 22:399–419

    Article  Google Scholar 

  • Corcelli A, Lattanzio VMT, Mascolo G, Babudri F, Oren A, Kates M (2004) Novel sulfonolipid in the extremely halophilic bacterium Salinibacter ruber. Appl Environ Microbiol 70:6678–6685

    Article  PubMed  CAS  Google Scholar 

  • Denger K, Cook AM (2001) Ethanedisulfonate is degraded via sulfoacetaldehyde in Ralstonia sp. strain EDS1. Arch Microbiol 176:89–95

    Article  PubMed  CAS  Google Scholar 

  • Denger K, Laue H, Cook AM (1997) Anaerobic taurine oxidation: a novel reaction by a nitrate-reducing Alcaligenes sp. Microbiology (Reading) 143:1919–1924

    CAS  Google Scholar 

  • Denger K, Smits THM, Cook AM (2006) l-Cysteate sulfo-lyase, a widespread, pyridoxal 5′-phosphate-coupled desulfonative enzyme purified from Silicibacter pomeroyi DSS-3T. Biochem J. DOI 10.1042/BJ20051311

  • Eichhorn E, Leisinger T (2001) Escherichia coli utilizes methanesulfonate and l-cysteate as sole sulfur sources for growth. FEMS Microbiol Lett 205:271–275

    PubMed  CAS  Google Scholar 

  • Eichhorn E, van der Ploeg JR, Leisinger T (2000) Deletion analysis of the Escherichia coli taurine and alkanesulfonate transport systems. J Bacteriol 182:2687–2795

    Article  PubMed  CAS  Google Scholar 

  • Fischer FG, Brander J (1960) Eine Analyse der Gespinste der Kreuzspinne. Hoppe-Seyler’s Z Physiol Chem 320:92–102

    PubMed  CAS  Google Scholar 

  • González JM, Covert JS, Whitman WB, Henriksen JR, Mayer F, Scharf B, Schmitt R, Buchan A, Fuhrman JA, Kiene RP, Moran MA (2003) Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int J Syst Evol Microbiol 53:1261–1269

    Article  PubMed  CAS  Google Scholar 

  • Graham DE, White RH (2002) Elucidation of methanogenic coenzyme biosyntheses: from spectroscopy to genomics. Nat Prod Rep 19:133–147

    Article  PubMed  CAS  Google Scholar 

  • Graham DE, Xu H, White RH (2002) Identification of coenzyme M biosynthetic phosphosulfolactate synthase: a new family of sulfonate biosynthesizing enzymes. J Biol Chem 277:13421–13429

    Article  PubMed  CAS  Google Scholar 

  • Guion-Rain MC, Portemer C, Chatagner F (1975) Rat liver cysteine sulfinate decarboxylase: purification, new appraisal of the molecular weight and determination of catalytic properties. Biochim Biophys Acta 384:265–276

    PubMed  CAS  Google Scholar 

  • Huxtable RJ (1992) Physiological actions of taurine. Physiol Rev 72:101–163

    PubMed  CAS  Google Scholar 

  • Kappler U, Bennett B, Rethmeier J, Schwarz G, Deutzmann R, McEwan AG, Dahl C (2000) Sulfite:Cytochrome c oxidoreductase from Thiobacillus novellus. Purification, characterization, and molecular biology of a heterodimeric member of the sulfite oxidase family. J Biol Chem 275:13202–13212

    Article  PubMed  CAS  Google Scholar 

  • Kappler U, Dahl C (2001) Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol Lett 203:1–9

    Article  PubMed  CAS  Google Scholar 

  • Kelly DP, Murrell JC (1999) Microbial metabolism of methanesulfonic acid. Arch Microbiol 172:341–348

    Article  PubMed  CAS  Google Scholar 

  • Kertesz MA (2000) Riding the sulfur cycle—metabolism of sulfonates and sulfate esters in gram-negative bacteria. FEMS Microbiol Rev 24:135–175

    PubMed  CAS  Google Scholar 

  • Khademi S, O’Connell J 3rd, Remis J, Robles-Colmenares Y, Miercke LJ, Stroud RM (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 A. Science 305:1587–1594

    Article  PubMed  CAS  Google Scholar 

  • Laue H, Denger K, Cook AM (1997a) Fermentation of cysteate by a sulfate-reducing bacterium. Arch Microbiol 168:210–214

    Article  CAS  Google Scholar 

  • Laue H, Denger K, Cook AM (1997b) Taurine reduction in anaerobic respiration of Bilophila wadsworthia RZATAU. Appl Environ Microbiol 63:2016–2021

    CAS  Google Scholar 

  • Lie TJ, Godchaux W, Leadbetter ER (1999) Sulfonates as terminal electron acceptors for growth of sulfite-reducing bacteria (Desulfitobacterium spp.) and sulfate-reducing bacteria: effects of inhibitors of sulfidogenesis. Appl Environ Microbiol 65:4611–4617

    PubMed  CAS  Google Scholar 

  • Lie TJ, Pitta T, Leadbetter ER, Godchaux III W, Leadbetter JR (1996) Sulfonates: novel electron acceptors in anaerobic respiration. Arch Microbiol 166:204–210

    Article  PubMed  CAS  Google Scholar 

  • Lie TL, Leadbetter JR, Leadbetter ER (1998) Metabolism of sulfonic acids and other organosulfur compounds by sulfate-reducing bacteria. Geomicrobiol J 15:135–149

    Article  CAS  Google Scholar 

  • Metzler DE (1977) Biochemistry: the chemical reactions of living cells. Academic, New York

    Google Scholar 

  • Metzler DE (2003) Biochemistry: the chemical reactions of living cells, 2nd edn. Academic, Amsterdam

    Google Scholar 

  • Mikosch C, Denger K, Schäfer E-M, Cook AM (1999) Anaerobic oxidations of cysteate: degradation via a cysteate:2-oxoglutarate aminotransferase in Paracoccus pantotrophus. Microbiology (Reading) 145:1153–1160

    CAS  Google Scholar 

  • Moran MA, Buchan A, González JM, Heidelberg JF, Whitman WB, Klene RP, Henriksen JR, King GM, Belas R, Fuqua C, Brinkac L, Lewis M, Johri S, Weaver B, Pal G, Eisen J, Rahe E, Sheldon WM, Ye W, Miller TR, Carlton J, Rasko DA, Paulsen IT, Ren Q, Dougherty SC, DeBoy RT, Dobson RJ, Durkin AS, Madupu R, Nelson WC, Sullivan SA, Rosovitz MJ, Haft DH, Selengut J, Ward N (2004) Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature (London) 432:910–913

    Article  CAS  Google Scholar 

  • Reichenbecher W, Kelly DP, Murrell JC (1999) Desulfonation of propanesulfonic acid by Comamonas acidovorans strain P53: evidence for an alkanesulfonate sulfonatase and an atypical sulfite dehydrogenase. Arch Microbiol 172:387–392

    Article  PubMed  CAS  Google Scholar 

  • Rein U, Gueta R, Denger K, Ruff J, Hollemeyer K, Cook AM (2005) Dissimilation of cysteate via 3-sulfolactate sulfo-lyase and a sulfate exporter in Paracoccus pantotrophus NKNCYSA. Microbiology (Reading) 151:737–747

    Article  CAS  Google Scholar 

  • Roy AB, Hewlins MJE, Ellis AJ, Harwood JL, White GF (2003) Glycolytic breakdown of sulfoquinovose in bacteria: a missing link in the sulfur cycle. Appl Environ Microbiol 69:6434–6441

    Article  PubMed  CAS  Google Scholar 

  • Scott LJ, Figgitt DP, Keam SJ, Waugh J (2005) Acamprosate: a review of its use in the maintenance of abstinence in patients with alcohol dependence. CNS Drugs 19:445–464

    Article  PubMed  CAS  Google Scholar 

  • Stapley EO, Starkey RL (1970) Decomposition of cysteic acid and taurine by soil microorganisms. J Gen Microbiol 64:77–84

    CAS  Google Scholar 

  • Stipanuk MH (2004) Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. Annu Rev Nutr 24:539–577

    Article  PubMed  CAS  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  PubMed  Google Scholar 

  • Visscher PT, Gritzer RF, Leadbetter ER (1999) Low-molecular-weight sulfonates, a major substrate for sulfate reducers in marine microbial mats. Appl Environ Microbiol 65:3272–3278

    PubMed  CAS  Google Scholar 

  • Weinstein CL, Griffith OW (1988) Cysteinesulfonate and β-sulfopyruvate metabolism. Partitioning between decarboxylation, transamination, and reduction pathways. J Biol Chem 263:3735–3743

    PubMed  CAS  Google Scholar 

  • White RH (1984) Biosynthesis of the sulfonolipid 2-amino-3-hydroxy-15-methylhexadecane-1-sulfonic acid in the gliding bacterium Cytophaga johnsonae. J Bacteriol 159:42–46

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Martha H. Stipanuk and John E. Dominy (Cornell University, Ithaca, NY, USA) for their advice on mammalian taurine synthesis. Much practical work in the authors’ lab was done by Andzelika Gorzynska, Ronnie Gueta, Heike Laue, Jutta Mayer, Ulrike Rein and Jürgen Ruff with funding from the University of Konstanz, the Deutsche Forschungsgemeinschaft, the European Union (SUITE: ENV4-CT98-0723), the LBS Stiftung ‘Umwelt und Wohnen’ and IAESTE.

Author information

Authors and Affiliations

  1. Department of Biology, The University of Konstanz, 78457, Konstanz, Germany

    Alasdair M. Cook, Karin Denger & Theo H. M. Smits

Authors
  1. Alasdair M. Cook
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karin Denger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Theo H. M. Smits
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alasdair M. Cook.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cook, A.M., Denger, K. & Smits, T.H.M. Dissimilation of C3-sulfonates. Arch Microbiol 185, 83–90 (2006). https://doi.org/10.1007/s00203-005-0069-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-005-0069-1

Keywords

Search

Navigation