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Characterization and identification of genes essential for dimethyl sulfide utilization in Pseudomonas putida strain DS1

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Abstract

Microbial dimethyl sulfide (DMS) conversion is thought to be involved in the global sulfur cycle. We isolated Pseudomonas putida strain DS1 from soil as a bacterium utilizing DMS as a sole sulfur source, and tried to elucidate the DMS conversion mechanism of strain DS1 at biochemical and genetic level. Strain DS1 oxidized DMS to dimethyl sulfone (DMSO2) via dimethyl sulfoxide, whereas the oxidation was repressed in the presence of sulfate, suggesting that a sulfate starvation response is involved in DMS utilization by strain DS1. Two of the five DMS-utilization-defective mutants isolated by transposon5 (Tn5) mutagenesis had a Tn5 insertion in the ssuEADCBF operon, which has been reported to encode a two-component monooxygenase system (SsuED), an ABC-type transporter (SsuABC), and a small protein (SsuF), and also to play a key role in utilization of sulfonates and sulfate esters in another bacterium, P. putida strain S-313. Disruption of ssuD and SsuD enzymatic activity demonstrated that methanesulfonate is a metabolic intermediate of DMS and desulfonated by SsuD. Disruption of ssuC or ssuF also led to a DMS-utilization-defective phenotype. Another two mutants had a defect in a gene homologous to pa2354 from P. aeruginosa PAO1, which encodes a putative transcriptional regulator, while the remaining mutant had a defect in cysM encoding O-acetylserine (thiol)-lyase B.

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References

  • Altschul SF, Madden TL, Schäffer AA, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    PubMed  Google Scholar 

  • Anzai Y, Kudo Y, Oyaizu H (1997) The phylogeny of the genera Chryseomonas, Flavimonas, and Pseudomonas supports synonymy of these three genera. Int J Syst Bacteriol 47:249–251

    CAS  PubMed  Google Scholar 

  • Bates TS, Charlson RJ, Gammon RH (1987) Evidence for the climatic role of marine biogenic sulfur. Nature 329:319–321

    CAS  Google Scholar 

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

    Google Scholar 

  • Coppée J-Y, Auger S, Turlin E, Sekowska A, Le Caer J-P, Labas V, Vanger V, Danchin A, Martin-Verstraete I (2001) Sulfur-limitation-regulated proteins in Bacillus subtilis: a two-dimensional gel electrophoresis study. Microbiology 147:1631–1640

    PubMed  Google Scholar 

  • De Bont JAM, van Dijken JP, Harder W (1981) Dimethylsulfoxide and dimethylsulfide as a carbon, sulfur and energy source for growth of Hyphomicrobium S. J Gen Microbiol 127:315–323

    Google Scholar 

  • Denome SA, Oldfield C, Nash LJ, Young KD (1994) Characterization of the desulfurization genes from Rhodococcus sp. strain IGTS8. J Bacteriol 176:6707–6716

    PubMed  Google Scholar 

  • De Souza MP, Yoch DC (1995) Purification and characterization of dimethylsulfoniopropionate lyase from an Alcaligenes-like dimethyl sulfide producing marine isolate. Appl Environ Microbiol 61:21–26

    Google Scholar 

  • Eichhorn E, van der Ploeg JR, Leisinger T (1999) Characterization of a two-component alkanesulfonate monooxygenase from Escherichia coli. J Biol Chem 274:26639–26646

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Endoh T, Habe H, Yoshida T, Nojiri H, Omori T (2003) A CysB-regulated and O54-dependent regulator, sfnR, is essential for dimethyl sulfone metabolism of Pseudomonas putida strain DS1. Microbiology DOI 10.1099/mic.0.26031-0

  • 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 66:5527–5532

    Article  CAS  PubMed  Google Scholar 

  • 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 140:1953–1958

    CAS  Google Scholar 

  • 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 155:99–105

    Article  CAS  PubMed  Google Scholar 

  • Johnston JB, Murray K, Cain RB (1975) Microbial metabolism of aryl sulphonates: a re-assessment of colorimetric methods for the determination of sulphite and their use in measuring desulphonation of aryl and alkylbenzene sulphonates. Antonie Van Leeuwenhoek 41:493–511

    CAS  PubMed  Google Scholar 

  • Kahnert A, Vermeij P, Wietek C, James CP, Leisinger T, Kertesz MA (2000) The ssu locus plays a key role in organosulfur metabolism in Pseudomonas putida S-313. J Bacteriol 182:2869–2878

    Article  CAS  PubMed  Google Scholar 

  • Kahnert A, Mirleau P, Wait R, Kertesz MA (2002) The LysR-type regulator SftR is involved in soil survival and sulphate ester metabolism in Pseudomonas putida. Environ Microbiol 4:225–237

    Article  CAS  PubMed  Google Scholar 

  • Kertesz MA (1999) Riding the sulfur cycle-metabolism of sulfonates and sulfate esters in Gram-negative bacteria. FEMS Microbiol Rev 24:135–175

    Article  Google Scholar 

  • Kertesz MA, Leisinger T, Cook AM (1993) Proteins induced by sulfate limitation in Escherichia coli, Pseudomonas putida, or Staphylococcus aureus. J Bacteriol 175:1187–1190

    CAS  PubMed  Google Scholar 

  • Kertesz MA, Schmidt-Larbig K, Wüest T (1999) A novel reduced flavin mononucleotide-dependent MS sulfonatase encoded by the sulfur-regulated msu operon of Pseudomonas aeruginosa. J Bacteriol 181:1464–1473

    CAS  PubMed  Google Scholar 

  • Ledyard KM, De Long EF, Dacey JWH (1993) Characterization of a DMSP-degrading bacterial isolate from Sargasso Sea. Arch Microbiol 160:312–318

    CAS  Google Scholar 

  • Li MZ, Squires CH, Monticello DJ, Childs JD (1996) Genetic analysis of the dsz promoter and associated regulatory regions of Rhodococcus erythropolis IGTS8. J Bacteriol 178:6409–6418

    CAS  PubMed  Google Scholar 

  • Lovelock JE, Maggs RJ, Rasmussen RA (1972) Atmospheric dimethylsulfide and the natural sulfur cycle. Nature 237:452–453

    CAS  Google Scholar 

  • Nakamura T, Kon Y, Igarashi H, Eguchi Y (1983) Evidence that thiosulfate assimilation by Salmonella typhimurium is catalyzed by cysteine synthase B. J Bacteriol 156:656–662

    CAS  PubMed  Google Scholar 

  • Ohshiro T, Hine Y, Izumi Y (1994) Enzymatic desulfurization of dibenzothiophene by a cell-free system of Rhodococcus erythropolis D-1. FEMS Microbiol Lett 118:341–344

    CAS  Google Scholar 

  • Oldfield C, Pogrebinsky O, Simmonds J, Olson ES, Kulpa CF (1997) Elucidation of the metabolic pathway for dibenzothiophene desulphurization by Rhodococcus sp. strain ITGS8 (ATCC53968). Microbiology 143:2961–2973

    PubMed  Google Scholar 

  • 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 Biotechol Biochem 59:1195–1198

    CAS  Google Scholar 

  • 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 5:105–112

    CAS  PubMed  Google Scholar 

  • Quadroni M, James P, Dainese-Hatt P, Kertesz MA (1999) Proteome mapping, mass spectrometric sequencing and reverse transcription-PCR for characterization of the sulfate starvation-induced response in Pseudomonas aeruginosa PAO1. Eur J Biochem 266:986–996

    CAS  PubMed  Google Scholar 

  • Rocha EPC, Sekowska A, Danchin A (2000) Sulfur island in the Escherichia coli genome: markers of the cell's architecture? FEBS Lett 476:8–11

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Sato S, Ouchiyama N, Kimura T, Nojiri H, Yamane H, Omori T (1997) Cloning of genes involved in carbazole degradation of Pseudomonas sp. strain CA10: nucleotide sequences of genes and characterization of meta-cleavage enzymes and hydrolase. J Bacteriol 179:4841–4849

    CAS  PubMed  Google Scholar 

  • Simon R, Priefer U, Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Biotechnology 1:784–791

    CAS  Google Scholar 

  • Sirko AE, Malgorzata M, Hulanicka MD (1987) Identification of the Escherichia coli cysM gene encoding O-acetylserine sulfhydrylase by cloning with min-Mu-lac containing a plasmid replicon. J Gen Microbiol 133:2719–2725

    CAS  PubMed  Google Scholar 

  • Smith NA, Kelly DP (1988a) Isolation and physiological characterization of autotrophic sulfur bacteria oxidizing dimethyl disulfide as sole source of energy. J Gen Microbiol 134:1407–1017

    CAS  Google Scholar 

  • Smith NA, Kelly DP (1988b) Mechanism of oxidation of dimethyl disulfide by Thiobacillus thioparus strain E6. J Gen Microbiol 134:3031–3039

    CAS  Google Scholar 

  • Stover KC, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1: an opportunistic pathogen. Nature 406:959–964

    Google Scholar 

  • Suylen GMH, Stefess GC, Kuenen JG (1986) Chemolithotrophic potential of a Hyphomicrobium species, capable of growth on methylated sulfur compounds. Arch Microbiol 146:192–198

    CAS  Google Scholar 

  • Van der Ploeg JR, Weiss MA, Saller E, Nashimoto H, Saito N, Kertesz MA, Leisinger T (1996) Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source. J Bacteriol 178:5438–5446

    PubMed  Google Scholar 

  • Visscher PT, van Gemerden H (1991) Photo-autotrophic growth of Thiocapsa roseopersicina on dimethyl sulfide. FEMS Microbiol Lett 81:247–250

    Article  CAS  Google Scholar 

  • Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24:263–290

    Article  CAS  PubMed  Google Scholar 

  • Yamano Y, Nishikawa T, Komatsu Y (1993) Cloning and nucleotide sequence of anaerobically induced porin protein E1 (OprE) of Pseudomonas aeruginosa PAO1. Mol Microbiol 8:993–1004

    PubMed  Google Scholar 

  • Yoshida T, Ayabe Y, Yasunaga M, Usami Y, Habe H, Nojiri H, Omori T (2003) Gene involved in the synthesis of the exopolysaccharide methanolan by the obligate methylotroph Methylobacillus sp. strain 12S. Microbiology 149:431–444

    Google Scholar 

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Acknowledgement

This work was supported in part by a Grant-in-Aid for Scientific Research (No. 14360050) to T. O. from the Ministry of Education, Science, Sports and Culture of Japan.

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Authors and Affiliations

  1. Biotechnology Research Center, The University of Tokyo, Bunkyo-ku, Yayoi 1–1–1, 113–8657, Tokyo, Japan

    T. Endoh, T. Yoshida, H. Habe, H. Nojiri & T. Omori

  2. Department of Biotechnology, Faculty of Bioresource Sciences, Akita Prefectural University, 247–7 Kaidobata-nishi, Shimoshinjo-nakano, 010–0195, Akita, Japan

    K. Kasuga

  3. Laboratory of Microbiology, Institute of Physical and Chemical Research (Riken), 2–1 Hirosawa, Wako-shi, 351–0198, Saitama, Japan

    M. Horinouchi

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  1. T. Endoh
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  2. K. Kasuga
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  3. M. Horinouchi
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Correspondence to T. Omori.

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Endoh, T., Kasuga, K., Horinouchi, M. et al. Characterization and identification of genes essential for dimethyl sulfide utilization in Pseudomonas putida strain DS1. Appl Microbiol Biotechnol 62, 83–91 (2003). https://doi.org/10.1007/s00253-003-1233-7

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  • DOI: https://doi.org/10.1007/s00253-003-1233-7

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