1887

Abstract

strain DS1 utilizes dimethyl sulfide (DMS) as a sulfur source, and desulfurizes it via dimethyl sulfoxide (DMSO), dimethyl sulfone (DMSO) and methanesulfonate (MSA). Its Tn mutant, Dfi74J, no longer utilized DMS, DMSO and DMSO, but could oxidize DMS to DMSO, suggesting that the conversion of DMSO to MSA was interrupted in the mutant. Sequencing of the Tn flanking region of Dfi74J demonstrated that a gene, (designated for dimethyl uloe utilization), encoding a transcriptional regulator containing an ATP-dependent σ-association domain and a DNA-binding domain, was disrupted. is part of an operon with two other genes, and , located immediately upstream of and in the same orientation. The genes encode NADH-dependent FMN reductase (SfnE) and FMNH-dependent monooxygenase (SfnC). Complementation of Dfi74J with an -expressing plasmid led to restoration of its growth on DMS, DMSO and DMSO. An -defective mutant of strain DS1, which lacks the factor, grew on MSA, but not on DMS, DMSO and DMSO, indicating that SfnR controls expression of gene(s) involved in DMSO metabolism by interaction with -RNA polymerase. Northern hybridization and a reporter gene assay with an transcriptional fusion elucidated that expression of the operon was induced under sulfate limitation and was dependent on a LysR-type transcriptional regulator, CysB. This is believed to be the first report that a -dependent transcriptional regulator induced under sulfate limitation is involved in sulfur assimilation.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26031-0
2003-04-01
2019-10-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/4/mic149991.html?itemId=/content/journal/micro/10.1099/mic.0.26031-0&mimeType=html&fmt=ahah

References

  1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, Z., Miller, W. & Lipman, D. J. ( 1997; ). Gapped BLAST and PSI-PLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402.[CrossRef]
    [Google Scholar]
  2. Autry, A. R. & Fitzgerald, J. W. ( 1990; ). Sulfonate S – a major form of forest soil organic sulfur. Biol Fertil Soils 10, 50–56.
    [Google Scholar]
  3. Bykowski, T., van der Ploeg, J. R., Iwanicka-Nowicka, R. & Hryniewicz, M. M. ( 2002; ). The switch from inorganic to organic sulphur assimilation in Escherichia coli: adenosine 5′-phosphosulphate (APS) as a signalling molecule for sulphate excess. Mol Microbiol 43, 1374–1358.
    [Google Scholar]
  4. Canellakis, E. S., Paterakis, A. A., Huang, S. C., Panagiotidis, C. A. & Kyriakidis, D. A. ( 1993; ). Identification, cloning, and nucleotide sequencing of the ornithine decarboxylase antizyme gene of Escherichia coli. Proc Natl Acad Sci U S A 90, 7129–7133.[CrossRef]
    [Google Scholar]
  5. Cases, I. & de Lorenzo, V. ( 2001; ). The limits to genomic predictions: role of σN in environmental stress survival of Pseudomonas putida. FEMS Microbiol Ecol 35, 217–221.
    [Google Scholar]
  6. Charlson, R. J., Lovelock, J. E., Andreae, M. O. & Warren, S. G. ( 1987; ). Oceanic phytoplankton, atmospheric sulfur, cloud albedo and climate. Nature 326, 655–661.[CrossRef]
    [Google Scholar]
  7. Chopra, A. K., Peterson, J. W. & Prasad, R. ( 1991; ). Cloning and sequence analysis of hydrogenase regulatory genes (hydHG) from Salmonella typhimurium. Biochim Biophys Acta 1129, 115–118.[CrossRef]
    [Google Scholar]
  8. Davison, J., Brunel, F., Phanopoulos, A., Prozzi, D. & Terpstra, P. ( 1992; ). Cloning and sequence of Pseudomonas genes determining sodium dodecyl sulfate biodegradation. Gene 114, 19–24.[CrossRef]
    [Google Scholar]
  9. de Bont, J. A. M., Van Dijken, J. P. & Harder, W. ( 1981; ). Dimethyl sulphoxide and dimethyl sulphide as a carbon, sulphur and energy source for growth of Hyphomicrobium S. J Gen Microbiol 127, 315–323.
    [Google Scholar]
  10. Denome, S. A., Oldfield, C., Nash, L. J. & Young, K. D. ( 1994; ). Characterization of the desulfurization genes from Rhodococcus sp. strain IGTS8. J Bacteriol 176, 6707–6716.
    [Google Scholar]
  11. 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 (in press). http://dx.doi.org/10.1007/s00253-003-1233-7
    [Google Scholar]
  12. Fitzgerald, J. W. ( 1976; ). Sulfate ester formation and hydrolysis: a potentially important yet often ignored aspect of the sulfur cycle of aerobic soils. Bacteriol Rev 40, 628–721.
    [Google Scholar]
  13. 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.[CrossRef]
    [Google Scholar]
  14. 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.[CrossRef]
    [Google Scholar]
  15. Hummerjohann, J., Küttel, E., Quadroni, M., Ragaller, J., Leisinger, T. & Kertesz, M. A. ( 1998; ). Regulation of the sulfate starvation response in Pseudomonas aeruginosa: role of cysteine biosynthetic intermediates. Microbiology 144, 1375–1386.[CrossRef]
    [Google Scholar]
  16. Hummerjohann, J., Laudenbach, S., Retey, J., Leisinger, T. & Kertesz, M. A. ( 2000; ). The sulfur-regulated arylsulfatase gene cluster of Pseudomonas aeruginosa, a new member of the cys regulon. J Bacteriol 182, 2055–2008.[CrossRef]
    [Google Scholar]
  17. Ishii, Y., Konishi, J., Okada, H., Hirasawa, K., Onaka, T. & Suzuki, M. ( 2000; ). Operon structure and functional analysis of the genes encoding thermophilic desulfurizing enzymes of Paenibacillus sp. A11-2. Biochem Biophys Res Commun 270, 81–88.[CrossRef]
    [Google Scholar]
  18. Kahnert, A., Vermeij, P., Wietek, C., James, P., Leisinger, T. & Kertesz, M. A. ( 2000; ). The ssu locus plays a key role in organosulfur metabolism in Pseudomonas putida S-313. J Bacteriol 182, 2869–2878.[CrossRef]
    [Google Scholar]
  19. Kahnert, A., Mirleau, P., Wait, R. & Kertesz, M. A. ( 2002; ). The LysR-type regulator SftR is involved in soil survival and sulphate ester metabolism in Pseudomonas putida. Environ Microbiol 4, 225–237.[CrossRef]
    [Google Scholar]
  20. Kertesz, M. A. ( 1999; ). Riding the sulfur cycle – metabolism of sulfonates and sulfate esters in Gram-negative bacteria. FEMS Microbiol Rev 24, 135–175.
    [Google Scholar]
  21. Kertesz, M. A., Schmidt-Larbig, K. & Wüest, T. ( 1999; ). A novel reduced flavin mononucleotide-dependent methanesulfonate sulfonatase encoded by the sulfur-regulated msu operon of Pseudomonas aeruginosa. J Bacteriol 181, 1464–1473.
    [Google Scholar]
  22. Köhlter, T., Harayama, S., Ramos, J.-L. & Timmis, K. N. ( 1989; ). Involvement of Pseudomonas putida RpoN σ factor in regulation of various metabolic functions. J Bacteriol 171, 4326–4333.
    [Google Scholar]
  23. Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., II & Peterson, K. M. ( 1995; ). Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166, 175–176.[CrossRef]
    [Google Scholar]
  24. Lomans, B. P., van der Drift, C., Pol, A. & Op den Camp, H. J. M. ( 2002; ). Microbial cycling of volatile organic sulfur compounds. Cell Mol Life Sci 59, 575–588.[CrossRef]
    [Google Scholar]
  25. Lovelock, J. E., Maggs, R. J. & Rasmussen, R. A. ( 1972; ). Atmospheric dimethylsulfide and the natural sulfur cycle. Nature 237, 452–453.[CrossRef]
    [Google Scholar]
  26. Marques, M. V., Gomes, S. L. & Gober, J. W. ( 1997; ). A gene coding for a putative sigma 54 activator is developmentally regulated in Caulobacter crescentus. J Bacteriol 179, 5502–5510.
    [Google Scholar]
  27. Miller, J. H. ( 1992; ). A Short Course in Bacterial Genetics, pp. 268–274, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  28. 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, 1195–1198.[CrossRef]
    [Google Scholar]
  29. Pandza, S., Baetens, M., Park, C. H., Au, T., Keyhan, M. & Matin, A. ( 2000; ). The G-protein FlhF has a role in polar flagellar placement and general stress response induction in Pseudomonas putida. Mol Microbiol 36, 414–423.[CrossRef]
    [Google Scholar]
  30. Quadroni, M., Staudenmann, M., Kertesz, M. A. & James, P. ( 1996; ). Analysis of global responses by protein and peptide fingerprinting of protein isolated by two-dimensional gel electrophoresis: application to the sulfate-starvation response of Escherichia coli. Eur J Biochem 239, 773–781.[CrossRef]
    [Google Scholar]
  31. Quadroni, M., James, P., Dainese-Hatt, P. & Kertesz, M. A. ( 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.[CrossRef]
    [Google Scholar]
  32. Ramos, J.-L., Marques, S. & Timmis, K. N. ( 1997; ). Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through an interplay of host factors and plasmid-encoded regulators. Annu Rev Microbiol 51, 341–373.[CrossRef]
    [Google Scholar]
  33. Reitzer, L. & Schneider, B. L. ( 2001; ). Metabolic context and possible physiological themes of σ54-dependent genes in Escherichia coli. Microbiol Mol Biol Rev 65, 422–444.[CrossRef]
    [Google Scholar]
  34. Rist, M. & Kertesz, M. A. ( 1998; ). Construction of improved plasmid vectors for promoter characterization in Pseudomonas aeruginosa and other Gram-negative bacteria. FEMS Microbiol Lett 169, 179–183.[CrossRef]
    [Google Scholar]
  35. Roberts, R. B., Abelson, P. H., Cowie, D. B., Bolton, E. T. & Britten, R. J. ( 1955; ). Studies of Biosynthesis in Escherichia coli, Washington, DC: Carnegie Institution.
  36. Rombel, I., North, A., Hwang, I., Wyman, C. & Kustu, S. ( 1998; ). The bacterial enhancer-binding protein NtrC as a molecular machine. Cold Spring Harbor Symp Quant Biol 63, 157–166.[CrossRef]
    [Google Scholar]
  37. Sambrook, J., Fritsch, E. F. &, Maniatis. T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  38. 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.
    [Google Scholar]
  39. Shingler, V., Bartilson, M. & Moore, T. ( 1993; ). Cloning and nucleotide sequence of the gene encoding the positive regulator (DmpR) of the phenol catabolic pathway encoded by pVI150 and identification of DmpR as a member of the NtrC family of transcriptional activators. J Bacteriol 175, 1596–1604.
    [Google Scholar]
  40. Simons, R. W., Houman, F. & Kleckner, N. ( 1987; ). Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53, 85–96.[CrossRef]
    [Google Scholar]
  41. Smith, N. A. & Kelly, D. P. ( 1988; ). Isolation and physiological characterization of autotrophic sulfur bacteria oxidizing dimethyl sulfide as sole source of energy. J Gen Microbiol 134, 1407–1417.
    [Google Scholar]
  42. Stover, K. C., Pham, X. Q., Erwin, A. L. & 28 other authors ( 2000; ). Complete genome sequence of Pseudomonas aeruginosa PAO1: an opportunistic pathogen. Nature 406, 959–964.[CrossRef]
    [Google Scholar]
  43. Uria-Nickelsen, M. R., Leadbetter, E. R. & Godchaux, W., III. ( 1993; ). Sulphonate utilization by enteric bacteria. J Gen Microbiol 139, 203–208.[CrossRef]
    [Google Scholar]
  44. van der Ploeg, J. R., Weiss, M. A., Saller, E., Nashimoto, H., Saito, N., Kertesz, M. A. & 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.
    [Google Scholar]
  45. van der Ploeg, J. R., Iwanicka-Nowicka, R., Kertesz, M. A., Leisinger, T. & Hryniewicz, M. M. ( 1997; ). Involvement of CysB and Cbl regulatory proteins in expression of the tauABCD operon and other sulfate starvation-inducible genes in Escherichia coli. J Bacteriol 179, 7671–7678.
    [Google Scholar]
  46. van der Ploeg, J. R., Cummings, N. J., Leisinger, T. & Connerton, I. F. ( 1998; ). Bacillus subtilis genes for the utilization of sulfur from aliphatic sulfonates. Microbiology 144, 2555–2561.[CrossRef]
    [Google Scholar]
  47. van der Ploeg, J. R., Iwanicka-Nowicka, R., Bykowski, T., Hryniewicz, M. M. & Leisinger, T. ( 1999; ). The Escherichia coli ssuEADCB gene cluster is required for the utilization of sulfur from aliphatic sulfonates and is regulated by the transcriptional activator Cbl. J Biol Chem 274, 29358–29365.[CrossRef]
    [Google Scholar]
  48. Vermeij, P., Wietek, C., Kahnert, A., Wüest, T. & Kertesz, M. A. ( 1999; ). Genetic organization of sulfur-controlled aryl desulfonation in Pseudomonas putida S-313. Mol Microbiol 32, 913–926.[CrossRef]
    [Google Scholar]
  49. Wardhan, H., McPherson, M. J. & Sastry, G. R. ( 1989; ). Identification, cloning, and sequence analysis of the nitrogen regulation gene ntrC of Agrobacterium tumefaciens C58. Mol Plant-Microbe Interact 2, 241–248.[CrossRef]
    [Google Scholar]
  50. Welsh, D. T. ( 2000; ). Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 24, 263–290.[CrossRef]
    [Google Scholar]
  51. Yoshida, T., Ayabe, Y., Yasunaga, M., Usami, Y., Habe, H., Nojiri, H. & Omori, T. ( 2003; ). Genes involved in the synthesis of the exopolysaccharide methanolan by the obligate methylotroph Methylobacillus sp. strain 12S. Microbiology 149, 431–444.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26031-0
Loading
/content/journal/micro/10.1099/mic.0.26031-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error