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Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes

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Abstract

In the phototrophic sulfur bacterium Allochromatium vinosum, sulfur of oxidation state zero stored in intracellular sulfur globules is an obligate intermediate during the oxidation of sulfide and thiosulfate. The proteins encoded in the dissimilatory sulfite reductase (dsr) locus are essential for the oxidation of the stored sulfur. DsrMKJOP form a membrane-spanning complex proposed to accept electrons from or to deliver electrons to cytoplasmic sulfur-oxidizing proteins. In frame deletion mutagenesis showed that each individual of the complex-encoding genes is an absolute requirement for the oxidation of the stored sulfur in Alc. vinosum. Complementation of the ΔdsrJ mutant using the conjugative broad host range plasmid pBBR1-MCS2 and the dsr promoter was successful. The importance of the DsrMKJOP complex is underlined by the fact that the respective genes occur in all currently sequenced genomes of sulfur-forming bacteria such as Thiobacillus denitrificans and Chlorobaculum tepidum. Furthermore, closely related genes are present in the genomes of sulfate- and sulfite-reducing prokaryotes. A phylogenetic analysis showed that most dsr genes from sulfide oxidizers are clearly separated of those from sulfate reducers. Surprisingly, the dsrMKJOP genes of the Chlorobiaceae all cluster together with those of the sulfate/sulfite-reducing prokaryotes, indicating a lateral gene transfer at the base of the Chlorobiaceae.

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References

  • Adachi J, Hasegawa M (1992) MOLPHY: programs for molecular phylogenetics, I. PROML: maximum likelihood inference of protein phylogeny. Institute of Statistical Mathematics, Tokyo, Japan

    Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, 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

    Article  PubMed  CAS  Google Scholar 

  • Ausubel FA, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1997) Current protocols in molecular biology. Wiley, New York

    Google Scholar 

  • Bazaral M, Helinski DR (1968) Circular DNA forms of colicinogenic factors E1, E2 and E3 from Escherichia coli. J Mol Biol 36:185–194

    Article  PubMed  CAS  Google Scholar 

  • Beller HR, Chai PSG, Letain TE, Chakicherla A, Larimer FW, Richardson PM, Coleman MA, Wood AP, Kelly DP (2006) The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriol 188:1473–1488

    Article  PubMed  CAS  Google Scholar 

  • Brune DC (1995) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, pp 847–870

    Google Scholar 

  • Dahl C (1996) Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum. Microbiology 142:3363–3372

    PubMed  CAS  Google Scholar 

  • Dahl C, Engels S, Pott-Sperling AS, Schulte A, Sander J, Lübbe Y, Deuster O, Brune DC (2005) Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J Bacteriol 187:1392–1404

    Article  PubMed  CAS  Google Scholar 

  • Dahl C, Prange A, Steudel R (2002) Natural polymeric sulfur compounds. In: Steinbüchel A (ed) Micscellaneous bioploymers and biodegradation of synthetic polymers. Wiley-VCH, Weinheim, pp 35–62

    Google Scholar 

  • Dahl C, Rákhely G, Pott-Sperling AS, Fodor B, Takács M, Tóth A, Kraeling M, Györfi K, Kovács A, Tusz J, Kovács K (1999) Genes involved in hydrogen and sulfur metabolism in phototrophic sulfur bacteria. FEMS Microbiol Lett 180:317–324

    Article  PubMed  CAS  Google Scholar 

  • Dahl C, Speich N, Trüper HG (1994) Enzymology and molecular biology of sulfate reduction in the extremely thermophilic archaeon Archaeoglobus fulgidus. Meth Enzymol 243:331–349

    Article  PubMed  CAS  Google Scholar 

  • Drake HL, Daniel SL (2004) Physiology of the thermophilic acetogen Moorella thermoacetica. Res Microbiol 155:869–883

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580

    Article  PubMed  CAS  Google Scholar 

  • Harmsen HJ, Van Kuijk BL, Plugge CM, Akkermans AD, de Vos WM, Stams AJ (1998) Syntrophobacter fumaroxidans sp. nov., a syntrophic propionate-degrading sulfate-reducing bacterium. Int J Syst Bacteriol 48:1383–1387

    CAS  Google Scholar 

  • Horton RM (1995) PCR mediated recombination and mutagenesis: SOEing together tailor-made genes. Mol Biotechnol 3:93–99

    PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314

    Article  PubMed  CAS  Google Scholar 

  • Jain R, Rivera M, Lake JA (2003) Horizontal gene transfer in microbial genome evolution. Theor Popul Biol 61:489–495

    Article  Google Scholar 

  • Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RMII, Peterson KM (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175–176

    Article  PubMed  CAS  Google Scholar 

  • Lübbe YJ, Youn H-S, Timkovich R, Dahl C (2006) Siro(haem)amide in Allochromatium vinosum and relevance of DsrL and DsrN, a homolog of cobyrinic acid a,c diamide synthase, for sulphur oxidation. FEMS Microbiol Lett (in press). DOI 10.1111/j.1574-6968.2006.00343.x

  • Mander GJ, Duin EC, Linder D, Stetter KO, Hedderich R (2002) Purification and characterization of a membrane-bound enzyme complex from the sulfate-reducing archaeon Archaeoglobus fulgidus related to heterodisulfide reductase from methanogenic archaea. Eur J Biochem 269:1895–1904

    Article  PubMed  CAS  Google Scholar 

  • Mussmann M, Richter M, Lombardot T, Meyerdierks A, Kuever J, Kube M, Glöckner FO, Amann R (2005) Clustered genes related to sulfate respiration in uncultured prokaryotes support the theory of their concomittant horizontal transfer. J Bacteriol 187:7126–7137

    Article  PubMed  CAS  Google Scholar 

  • Page PD (1996) Tree-View: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Pattaragulwanit K, Dahl C (1995) Development of a genetic system for a purple sulfur bacterium: conjugative plasmid transfer in Chromatium vinosum. Arch Microbiol 164:217–222

    Article  CAS  Google Scholar 

  • Pires RH, Venceslau SS, Morais F, Teixeira M, Xavier AV, Pereira IAC (2006) Characterization of the Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP complex—a membrane-bound redox complex involved in the sulfate respiratory pathway. Biochemistry 45:249–262

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Pott AS, Dahl C (1998) Sirohaem-sulfite reductase and other proteins encoded in the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology 144:1881–1894

    Article  PubMed  CAS  Google Scholar 

  • Prange A, Engelhardt H, Trüper HG, Dahl C (2004) The role of the sulfur globule proteins of Allochromatium vinosum: mutagenesis of the sulfur globule protein genes and expression studies by Real-time RT PCR. Arch Microbiol 182:165–174

    Article  PubMed  CAS  Google Scholar 

  • Rethmeier J, Rabenstein A, Langer M, Fischer U (1997) Detection of traces of oxidized and reduced sulfur compounds in small samples by combination of different high-performance liquid chromatography methods. J Chromatogr A 760:295–302

    Article  CAS  Google Scholar 

  • Rossi M, Pollock BR, Reiji MW, Keon RG, Fu R, Voordouw G (1993) The hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough encodes a potential transmembrane redox protein complex. J Bacteriol 175:4699–4711

    PubMed  CAS  Google Scholar 

  • Sabehi G, Loy A, Jung K-H, Partha R, Spudich JL, Isaacson T, Hirschberg J, Wagner M, Béjà O (2005) New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLOS Biology 3:1409–1417

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Schäfer A, Tauch A, Jäger W, Kalinowski J, Thierbach G, Pühler A (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69–73

    Article  PubMed  Google Scholar 

  • Seibl R, Höltke H-J, Rüger R, Meindl A, Zauchau HG, Raßhofer R, Wolf H, Arnold N, Wienberg J, Kessler C (1990) Nonradioactive labeling and detection of nucleic acids. Biol Chem Hoppe Seyler 371:939–951

    PubMed  CAS  Google Scholar 

  • Simmons SL, Sievert SM, Frankel RB, Bazylinski DA, Edwards KJ (2004) Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Appl Environ Microbiol 70:6230–6239

    Article  PubMed  CAS  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. Bio/Technology 1:784–791

    Article  CAS  Google Scholar 

  • Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (* and other methods), Version 4.0b 10. Sinauer Associates, Saunderland, MA

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, 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  CAS  Google Scholar 

  • Wagner M, Roger AJ, Flax JL, Brusseau GA, Stahl DA (1998) Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J Bacteriol 180:2975–2982

    PubMed  CAS  Google Scholar 

  • Weaver PF, Wall JD, Gest H (1975) Characterization of Rhodopseudomonas capsulata. Arch Microbiol 105:207–216

    Article  PubMed  CAS  Google Scholar 

  • Zverlov V, Klein M, Lücker S, Friedrich MW, Kellermann J, Stahl DA, Loy A, Wagner M (2005) Lateral gene transfer of dissimilatory (bi)sulfite reductase revisited. J Bacteriol 187:2203–2208

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grant Da 351/3–3 from the Deutsche Forschungsgemeinschaft. The excellent technical assistance by Birgitt Hüttig is gratefully acknowledged. We are indebted to Hans G. Trüper for the continuing support and the stimulating discussions.

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  1. Institut für Mikrobiologie und Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Meckenheimer Allee 168, 53115, Bonn, Germany

    Johannes Sander, Sabine Engels-Schwarzlose & Christiane Dahl

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  1. Johannes Sander
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  2. Sabine Engels-Schwarzlose
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  3. Christiane Dahl
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Correspondence to Christiane Dahl.

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Sander, J., Engels-Schwarzlose, S. & Dahl, C. Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes. Arch Microbiol 186, 357–366 (2006). https://doi.org/10.1007/s00203-006-0156-y

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  • DOI: https://doi.org/10.1007/s00203-006-0156-y

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