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
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
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
Boogerd F, De Vrind J (1987) Manganese oxidation by Leptothrix discophora. J Bacteriol 169:489–494
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
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
Collins P, Dobson A (1997) Regulation of laccase gene transcription in Trametes versicolor. Appl Environ Microbiol 63:3444–3450
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
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
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
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
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
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
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
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
Ghiorse W (1984) Biology of iron-and manganese-depositing bacteria. Annu Rev Microbiol 38:515–550
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
Malhorta K, Sharma P, Capalash N (2004) Copper and dyes enhance laccase production in alpha-proteobacterium JB. Biotechnol Lett 26:1047–1050
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
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
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
Stone A (1987) Microbial metabolites and the reductive dissolution of manganese oxides: oxalate and pyruvate. Geochim Cosmochim Acta 51:919–925
Sunda W, Kieber D (1994) Oxidation of humic substances by manganese oxides yields low-molecular-weight organic substrates. Nature 367:62–64
Tebo B (1991) Manganese(II) oxidation in the suboxic zone of the Black Sea. Deep Sea Res 38:S883–S905
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
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
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
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
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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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