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Two different electron transfer pathways may involve in azoreduction in Shewanella decolorationis S12

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Abstract

Electron transfer pathways for azoreduction by S. decolorationis S12 were studied using a mutant S12-22 which had a transposon insertion in ccmA. The results imply that there are two different pathways for electron transport to azo bonds. The colony of S12-22 was whitish and incapable of producing mature c-type cytochromes whose α-peak was at 553 nm in the wild type S12. The mutant S12-22 could not use formate as the sole electron donor for azoreduction either in vivo or in vitro, but intact cells of S12-22 were able to reduce azo dyes of low polarity, such as methyl red, when NADH was served as the sole electron donor. Although the highly polar-sulfonated amaranth could not be reduced by intact cells of S12-22, it could be efficiently reduced by cell extracts of the mutant when NADH was provided as the sole electron donor. These results suggest that the mature c-type cytochromes are essential electron mediators for the extracellular azoreduction of intact cells, while the other pathway without the involvement of mature c-type cytochromes, NADH-dependent oxidoreductase-mediated electron transfer pathway can reduce lowly polar sulfonated azo dyes inside the whole cells or highly polar sulfonated azo dyes in the cell extracts without bacterial membrane barriers.

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References

  • Alexeyev MF, Shokolenko IN (1995) Mini-Tn10 transposon derivatives for insertion mutagenesis and gene delivery into the chromosome of Gram-negative bacteria. Gene 160:59–62

    Article  CAS  Google Scholar 

  • Arnold RG, Dichristina TJ, Hoffmann MR (1986) Inhibitor studies of dissimilative Fe (III) reduction by Pseudomonas sp. strain 200 (“Pseudomonas ferrireductans”). Appl Environ Microbiol 52:281–289

    CAS  Google Scholar 

  • Bouhenni R, Gehrke A, Saffarini D (2005) Identification of genes involved in cytochrome c biogenesis in Shewanella oneidensis, using a modified mariner transposon. Appl Environ Microbiol 71:4935–4937

    Article  CAS  Google Scholar 

  • Brigé A, Motte B, Borloo J, Buysschaert G, Devreese B, Van Beeumen JJ (2008) Bacterial decolorization of textile dyes is an extracellular process requiring a multicomponent electron transfer pathway. Microb Biotechnol 1:40–52

    Google Scholar 

  • Fredrich E, Van Heek P, Leif H, Ohnishi T, Forche E, Kunze B, Jansen R, Trowitzsch-Kienast W, Hofle G, Reichenbach H, Weiss H (1994) Two binding sites of inhibitors in NADH: ubiquinone oxidoreductase (complex I). Eur J Biochem 219:691–698

    Article  Google Scholar 

  • Ghosh DK, Mandal A, Chaudhuri J (1992) Purification and partial characterization of two azoreductases from Shigella dysenteriae type 1. FEMS Microbiol Lett 77:229–233

    Article  CAS  Google Scholar 

  • Ghosh DK, Ghosh S, Sadhukhan P, Mandal A, Chaudhuri J (1993) Purification of two azoreductases from Escherichia coli K12. Indian J Exp Biol 31:951–954

    CAS  Google Scholar 

  • Goldmann BS, Gabbert KK, Kranz RG (1996) Use of heme reporters for studies of cytochrome biosynthesis and heme transport. J Bacteriol 178:6338–6347

    Google Scholar 

  • Groh JL, Luo Q, Ballard JD, Krumholz LR (2005) A method adapting microarray technology for signature-tagged mutagenesis of Desulfovibrio desulfuricans G20 and Shewanella oneidensis MR-1 in anaerobic sediment survival experiments. Appl Environ Microbiol 71:7064–7074

    Article  CAS  Google Scholar 

  • Gutman M, Singer TP, Beinert H, Casida JE (1970) Reaction sites of rotenone, piericidin A, and amytal in relation to the nonheme iron components of NADH dehydrogenase. Proc Natl Acad Sci USA 65:763–770

    Article  CAS  Google Scholar 

  • Heidelberg J, Paulsen I, Nealson K, Gaidos E, Nelson W, Read T et al (2002) Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol 20:1118–1123

    Article  CAS  Google Scholar 

  • Hong Y, Guo J, Xu Z, Xu M, Sun G (2007a) Humic substances act as electron acceptor and redox mediator for microbial dissimilatory azoreduction by Shewanella decolorationis S12. J Microbiol Biotechnol 17:428–437

    CAS  Google Scholar 

  • Hong Y, Xu M, Guo J, Xu Z, Chen X, Sun G (2007b) Respiration and growth of Shewanella decolorationis S12 with azo compound as sole electron acceptor. Appl Environ Microbiol 73:64–72

    Article  CAS  Google Scholar 

  • Horitsu H, Takada M, Idaka E, Tomoyeda M, Ogawa T (1977) Degradation of p-aminoazobenzene by Bacillus subtilis. Eur J Appl Microbiol 4:217–224

    Article  CAS  Google Scholar 

  • Ito K, Nakanishi M, Lee WC, Zhi Y, Sasaki H, Zenno S, Saigo K, Kitade Y, Tanokura M (2008) Expansion of substrate specificity and catalytic mechanism of azoreductase by X-ray crystallography and site-directed mutagenesis. J Biol Chem 283:13889–13896

    Article  CAS  Google Scholar 

  • Keck A, Klein J, Kudlich M, Stolz A, Knackmuss HJ, Mattes R (1997) Reduction of azo dyes by redox mediators originating in the naphthalenesulfonic acid degradation of Sphingom onas sp. strain BN6. Appl Environ Microbiol 63:3684–3690

    CAS  Google Scholar 

  • Kudlich M, Keck A, Klein J, Stolz A (1997) Localization of the enzyme system involved in anaerobic reduction of azo dyes by Sphingomonas sp. strain BN6 and effect of artificial redox mediators on the rate of azo dye reduction. Appl Environ Microbiol 63:3691–3694

    CAS  Google Scholar 

  • Maier J, Kandelbauer A, Erlacher A, Cavaco-Paulo A, Gubitz G (2004) A new alkali-thermostable azoreductase from Bacillus sp. strain SF. Appl Environ Microbiol 70:837–844

    Article  CAS  Google Scholar 

  • Meyer T, Tsapin A, Vandenberghe I, de Smet L, Frishman D, Nealson K, Cusanovich M, van Beeumen J (2004) Identification of 42 possible cytochrome c genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. OMICS 8:57–77

    Article  CAS  Google Scholar 

  • Moser D, Nealson K (1996) Growth of the facultative anaerobe Shewanella putrefaciens by elemental sulfur reduction. Appl Environ Microbiol 62:2100–2105

    CAS  Google Scholar 

  • Moutaouakkil A, Zeroual Y, Zohra-Dzayri F, Talbi M, Lee K, Blaghen M (2003) Purification and partial characterization of azoreductase from Enterobacter agglomerans. Arch Biochem Biophys 413:139–146

    Article  CAS  Google Scholar 

  • Myers CR, Carstens BP, Antholine WE, Myers JM (2000) Chromium (VI) reductase activity is associated with the cytoplasmic membrane of anaerobically grown Shewanella putrefaciens MR-1. J Appl Microbiol 88:98–106

    Article  CAS  Google Scholar 

  • Nakanishi M, Yatome C, Ishida N, Kitade Y (2001) Putative ACP phosphodiesterase gene (acpD) encodes an azoreductase. J Biol Chem 276:46394–46399

    Article  CAS  Google Scholar 

  • Nealson K, Saffarini D (1994) Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu Rev Microbiol 48:311–343

    Article  CAS  Google Scholar 

  • Rafii F, Cerniglia CE (1993) Comparison of the azoreductase and nitroreductase from Clostridium perfringens. Appl Environ Microbiol 59:1731–1734

    CAS  Google Scholar 

  • Ramalho PA, Paiva S, Cavaco-Paulo A, Casal M, Cardoso MH, Ramalho MT (2005) Azo reductase activity of intact Saccharomyces cerevisiae cells is dependent on the Fre1p component of plasma membrane ferric reductase. Appl Environ Microbiol 71:3882–3888

    Article  CAS  Google Scholar 

  • Rau J, Stolz A (2003) Oxygen-insensitive nitroreductases NfsA and NfsB of Escherichia coli function under anaerobic conditions as lawsone-dependent azo reductases. Appl Environ Microbiol 69:3448–3455

    Article  CAS  Google Scholar 

  • Russ R, Rau J, Stolz A (2000) The function of cytoplasmatic flavin reductases in the bacterial reduction of azo dyes. Appl Environ Microbiol 66:1429–1434

    Article  CAS  Google Scholar 

  • Saltikov CW, Cifuentes A, Venkateswaran K, Newman DK (2003) The ars detoxification system is advantageous but not required for As (V) respiration by the genetically tractable Shewanella species strain ANA-3. Appl Environ Microbiol 69:2800–2809

    Article  CAS  Google Scholar 

  • Stolz A (2001) Basic and applied aspects in the microbial degradation of azo dyes. Appl Microbiol Biotechnol 56:69–80

    Article  CAS  Google Scholar 

  • Suzuki Y, Yoda T, Ruhul A, Sugiura W (2001) Molecular cloning and characterization of the gene coding for azoreductase from Bacillus sp. OY1–2 isolated from soil. J Biol Chem 276:9059–9065

    Article  CAS  Google Scholar 

  • Thöny-Meyer L, Ritz D, Hennecke H (1994) Cytochrome c biogenesis in bacteria: a possible pathway begins to emerge. Mol Microbiol 12:1–9

    Article  Google Scholar 

  • Thöny-Meyer L, Fischer F, Kunzler P, Ritz D, Hennecke H (1995) Escherichia coli genes required for cytochrome c maturation. J Bacteriol 177:4321–4326

    Google Scholar 

  • Throne-Holst M, Thöny-Meyer L, Hederstedt L (1997) Escherichia coli ccm in-frame deletion mutants can produce periplasmic cytochrome b but not cytochrome c. FEBS Lett 410:351–355

    Article  CAS  Google Scholar 

  • Van der Zee FP, Bouwman RHM, Strik DPBTB, Lettinga G, Field JA (2001) Application of redox mediators to accelerate the transformation of reactive azo dyes in anaerobic bioreactors. Biotechnol Bioeng 75:691–701

    Article  Google Scholar 

  • Wade R, DiChristina T (2000) Isolation of U (VI) reduction-deficient mutants of Shewanella putrefaciens. FEMS Microbiol Lett 184:143–146

    Article  CAS  Google Scholar 

  • Zimmermann T, Kulla HG, Leisinger T (1982) Properties of purified orange II azoreductase, the enzyme initiating azo dye degradation by Pseudomonas KF46. Eur J Biochem 129:197–203

    Article  CAS  Google Scholar 

  • Zimmermann T, Gasser F, Kulla HG, Leisinger T (1984) Comparison of two bacterial azoreductases acquired during adaptation to growth on azo dyes. Arch Microbiol 138:37–43

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Chinese National Natural Science Foundation (30500009 and 30670020), Chinese National Programs for High Technology Research and Development (2006AA06Z322), and Natural Science Foundation Guangdong province (9351007002000001).

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Correspondence to Meiying Xu.

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Chen, X., Xu, M., Wei, J. et al. Two different electron transfer pathways may involve in azoreduction in Shewanella decolorationis S12. Appl Microbiol Biotechnol 86, 743–751 (2010). https://doi.org/10.1007/s00253-009-2376-y

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