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An uncertain role for Cu(II) in stimulating Mn(II) oxidation by Leptothrix discophora SS-1

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Abstract

In an effort to improve understanding of the role of Cu(II) in bacterial Mn(II) oxidation, a model Mn(II)-oxidizing bacterium, Leptothrix discophora SS-1, was grown in presence of toxic and non-toxic concentrations of Cu(II), Cd(II) and Mn(II). Mn(II)-oxidizing activity increased by 40% when cells were grown in the presence of 0.05 μM of Cu(II) and increased twofold at 0.18 μM Cu(II). Toxic levels of Cd(II) did not stimulate Mn(II) oxidizing activity, indicating that Mn(II) oxidation is not a response to metal toxicity. Stimulation by Cu(II) confirms the specific role of Cu(II) in Mn(II) oxidation. Comparison of transcript levels of the multicopper oxidase mofA gene in the presence and absence of added Cu(II) do not indicate a statistically significant change in mofA transcript levels in cultures supplemented with Cu(II). Thus, the exact role of Cu(II) in Mn(II) oxidation and its affect on mofA gene expression remain uncertain.

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References

  • Adams L, Ghiorse W (1985) Influence of manganese on growth of a sheathless strain of Leptothrix discophora. Appl Environ Microbiol 49:556–562

    CAS  PubMed  Google Scholar 

  • Adams L, Ghiorse W (1987) Characterization of extracellular Mn2+-oxidizing activity and isolation of an Mn2+-oxidizing protein from Leptothrix discophora SS-1. J Bacteriol 169:1279–1285

    CAS  PubMed  Google Scholar 

  • Anderson C, Johnson H, Caputo N, Davis R, Torpey J, Tebo B (2009) Mn(II) oxidation is catalyzed by heme peroxidases in “aurantimonas manganoxydans” strain SI85–9A1 and Erythrobacter sp. strain SD-21. Appl Environ Microbiol 75:4130–4138

    Article  CAS  PubMed  Google Scholar 

  • Boogerd F, De Vrind J (1987) Manganese oxidation by Leptothrix discophora. J Bacteriol 169:489–494

    CAS  PubMed  Google Scholar 

  • Brouwers G (1999) Molecular genetic aspects of microbial manganese oxidation: a geophysiological study. Ph.D. thesis; Leiden Institute of Chemistry. Leiden University, Leiden

  • Brouwers G (2000) Stimulation of Mn2+ oxidation in Leptothrix discophora SS-1 by Cu2+ and sequence analysis of the region flanking the gene encoding putative multicopper oxidase Mofa. Geomicrobiol J 17:25–33

    Article  CAS  Google Scholar 

  • Brouwers G, De Vrind J, Corstjens P, Cornelis P, Baysse C, De Vrind-De Jong E (1999) cumA, a gene encoding a multicopper oxidase, is involved in Mn2+ oxidation in Pseudomonas putida GB-1. Appl Environ Microbiol 65:1762–1768

    CAS  PubMed  Google Scholar 

  • Collins P, Dobson A (1997) Regulation of laccase gene transcription in Trametes versicolor. Appl Environ Microbiol 63:3444–3450

    CAS  PubMed  Google Scholar 

  • Corstjens P, De Vrind J, Westbroek P, De Vrind-De Jong E (1992) Enzymatic iron oxidation by Leptothrix discophora: identification of an iron-oxidizing protein. Appl Environ Microbiol 58:450–454

    CAS  PubMed  Google Scholar 

  • Corstjens P, De Vrind J, Goosen T, De Vrind-De Jong E (1997) Identification and molecular analysis of the Leptothrix discophora SS-1 mofA gene, a gene putatively encoding a manganese-oxidizing protein with copper domains. Geomicrobiol J 14:91–108

    Article  CAS  Google Scholar 

  • Dick G, Podell S, Johnson H, Rivera-Espinoza Y, Bernier-Latman R, Mccarthy J, Torpey J, Clement B, Gaasterland T, Tebo B (2008a) Genomic insights into Mn(II) oxidation by the marine Alphaproteobacterium Aurantimonas sp. strain SI85–9A1. Appl Environ Microbiol 74:2646–2658

    Article  CAS  PubMed  Google Scholar 

  • Dick G, Torpey J, Beveridge T, Tebo B (2008b) Direct Identification of a bacterial manganese(II) oxidase, the multicopper oxidase MnxG, from spores of several different marine Bacillus Species. Appl Environ Microbiol 74:1527–1534

    Article  CAS  PubMed  Google Scholar 

  • Dong D, Nelson Y, Lion L, Shuler M, Ghiorse W (2000) Adsorption of Pb and Cd onto metal oxides and organic material in natural surface coatings as determined by selective extractions: new evidence for the importance of Mn and Fe oxides. Water Res 34:427–436

    Article  CAS  Google Scholar 

  • El Gheriany I, Bocioaga D, Hay A, Ghiorse W, Shuler M, Lion L (2009) Iron requirement for Mn(II) oxidation by Leptothrix discophora SS-1. Appl Environ Microbiol 75:1229–1235

    Article  CAS  PubMed  Google Scholar 

  • Francis C, Casciotti K, Tebo B (2002) Localization of Mn(II)-oxidizing activity and the putative multicopper oxidase, MnxG, to the exosporium of the marine Bacillus sp. strain SG-1. Arch Microbiol 178:450–456

    Article  CAS  PubMed  Google Scholar 

  • Geszvain K, Tebo B (2010) Identification of a two-component regulatory pathway essential for Mn(II) oxidation in Pseudomonas putida GB-1. Appl Environ Microbiol 76:1224–1231

    Article  CAS  PubMed  Google Scholar 

  • Ghiorse W (1984) Biology of iron-and manganese-depositing bacteria. Annu Rev Microbiol 38:515–550

    CAS  PubMed  Google Scholar 

  • Larsen E, Sly L, Mcewan A (1999) Manganese(II) adsorption and oxidation by whole cells and a membrane fraction of Pedomicrobium sp. ACM 3067. Arch Microbiol 171:257–264

    Article  CAS  Google Scholar 

  • Malhorta K, Sharma P, Capalash N (2004) Copper and dyes enhance laccase production in alpha-proteobacterium JB. Biotechnol Lett 26:1047–1050

    Article  Google Scholar 

  • Nealson Kh, Tebo Bm, Rosson Ra, Allen Il (1988) Occurrence and mechanisms of microbial oxidation of manganese. In: Laskin A (ed) Advances in applied microbiology. Academic Press, pp 279–318

  • Nelson Y, Lion L, Shuler M, Ghiorse W (1999) Lead binding to metal oxide and organic phases of natural aquatic biofilms. Limnol Oceanogr 44:1715–1729

    Article  CAS  Google Scholar 

  • Palmieri G, Giardina P, Bianco C, Fontanella B, Sannia G (2000) Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl Environ Microbiol 66:920–924

    Article  CAS  PubMed  Google Scholar 

  • Ridge J, Lin M, Larsen E, Fegan M, Mcewan A, Sly L (2007) A multicopper oxidase is essential for manganese oxidation and laccase-like activity in Pedomicrobium sp. ACM 3067. Environ Microbiol 9:944–953

    Article  CAS  PubMed  Google Scholar 

  • Stone A (1987) Microbial metabolites and the reductive dissolution of manganese oxides: oxalate and pyruvate. Geochim Cosmochim Acta 51:919–925

    Article  CAS  Google Scholar 

  • Sunda W, Kieber D (1994) Oxidation of humic substances by manganese oxides yields low-molecular-weight organic substrates. Nature 367:62–64

    Article  CAS  Google Scholar 

  • Tebo B (1991) Manganese(II) oxidation in the suboxic zone of the Black Sea. Deep Sea Res 38:S883–S905

    Article  Google Scholar 

  • Tebo B, Bargar J, Clement B, Dick G, Murray K, Parker D, Verity R, Webb S (2004) Biogenic manganese oxides: properties and mechanisms of formation. Annu Rev Earth Planet Sci 32:287–328

    Article  CAS  Google Scholar 

  • Van Waasbergen L, Hildebrand M, Tebo B (1996) Identification and characterization of a gene cluster involved in manganese oxidation by spores of the marine Bacillus sp. strain SG-1. J Bacteriol 178:3517–3530

    PubMed  Google Scholar 

  • Wehrli B, Friedl G, Manceau A (1995) Reaction rates and products of manganese oxidation at the sediment-water interface. In: Huang CP, O'Melia CR, Morgan JJ (eds) Aquatic chemistry: interfacial and interspecies processes (Advances in chemistry series). American Chemical Society, Washington

  • Wilson C, Apiyo D, Wittung-Stafshede P (2004) Role of cofactors in metalloprotein folding. Q Rev Biophys 37:285–314

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Lion L, Nelson Y, Shuler M, Ghiorse W (2002) Kinetics of Mn(II) oxidation by Leptothrix discophora SS1. Geochim Cosmochim Acta 66:773–781

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by NSF grant EAR-0311767. The authors are grateful to Herdis Schopka for assistance with ICP-OES.

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Correspondence to Leonard W. Lion.

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Communicated by Gregory Cook.

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El Gheriany, I.A., Bocioaga, D., Hay, A.G. et al. An uncertain role for Cu(II) in stimulating Mn(II) oxidation by Leptothrix discophora SS-1. Arch Microbiol 193, 89–93 (2011). https://doi.org/10.1007/s00203-010-0645-x

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  • DOI: https://doi.org/10.1007/s00203-010-0645-x

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