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

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ORIGINAL PAPER

An uncertain role for Cu(II) in stimulating Mn(II) oxidation by Leptothrix discophora SS-1 Iman A. El Gheriany • Daniela Bocioaga Anthony G. Hay • William C. Ghiorse • Michael L. Shuler • Leonard W. Lion



Received: 22 April 2010 / Revised: 6 October 2010 / Accepted: 18 October 2010 / Published online: 10 November 2010 Ó Springer-Verlag 2010

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 lM of Cu(II) and increased twofold at 0.18 lM 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. Keywords Mn(II) oxidation  Leptothrix discophora  Copper  Transcript  mofA

Communicated by Gregory Cook. I. A. El Gheriany  M. L. Shuler School of Chemical and Biomolecular Engineering, Olin Hall, Cornell University, Ithaca, NY 14853, USA D. Bocioaga  A. G. Hay  W. C. Ghiorse Department of Microbiology, Wing Hall, Cornell University, Ithaca, NY 14853, USA L. W. Lion (&) School of Civil and Environmental Engineering, Hollister Hall, Cornell University, Ithaca, NY 14853, USA e-mail: [email protected]

Introduction Mn(III, IV) oxides greatly affect the biogeochemistry and the fundamental cycling process of many toxic and essential elements (Ghiorse 1984; Tebo et al. 2004). These highly reactive mineral phases are strong adsorbents of heavy metals and participate in a wide range of redox reactions (Stone 1987; Sunda and Kieber 1994; Nelson et al. 1999; Dong et al. 2000). At circumneutral pH values, the rate of formation of biologically formed Mn(III,IV) oxides is several orders of magnitude higher than the rate of chemical oxidation (Nealson et al. 1988; Tebo 1991; Wehrli et al. 1995). It is now widely accepted that Mn(II) oxidation kinetics are microbially mediated in aerobic natural waters (Tebo et al. 2004). Bacterial Mn(II) oxidation was found to be catalyzed by proteins containing conserved copper-binding motifs that are characteristic of multicopper oxidases e.g., MoxA in Pedomicrobium sp. ACM 3067 (Ridge et al. 2007) and MnxG in Bacillus spores SG-1 (van Waasbergen et al. 1996; Francis et al. 2002; Dick et al. 2008b) and by hemecontaining peroxidases (Anderson et al. 2009). In Leptothrix discophora SS-1, mofA is thought to encode for the Mn(II)-oxidizing factor. This gene was originally characterized by Corstjens et al