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Fungal oxidative dissolution of the Mn(II)-bearing mineral rhodochrosite and the role of metabolites in manganese oxide formation

Authors

  • Yuanzhi Tang,

    1. School of Engineering and Applied Sciences, Harvard University, Cambridge, MA, USA
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    • These authors contributed equally to this work.
  • Carolyn A. Zeiner,

    1. School of Engineering and Applied Sciences, Harvard University, Cambridge, MA, USA
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    • These authors contributed equally to this work.
  • Cara M. Santelli,

    1. Department of Mineral Sciences, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA
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  • Colleen M. Hansel

    Corresponding author
    • School of Engineering and Applied Sciences, Harvard University, Cambridge, MA, USA
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    • Present address: Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.

For correspondence. E-mail chansel@whoi.edu; Tel. (+1) 508 289 3858; Fax (+1) 508 457 2161.

Summary

Microbially mediated oxidation of Mn(II) to Mn(III/IV) oxides influences the cycling of metals and remineralization of carbon. Despite the prevalence of Mn(II)-bearing minerals in nature, little is known regarding the ability of microbes to oxidize mineral-hosted Mn(II). Here, we explored oxidation of the Mn(II)-bearing mineral rhodochrosite (MnCO3) and characteristics of ensuing Mn oxides by six Mn(II)-oxidizing Ascomycete fungi. All fungal species substantially enhanced rhodochrosite dissolution and surface modification. Mineral-hosted Mn(II) was oxidized resulting in formation of Mn(III/IV) oxides that were all similar to δ-MnO2 but varied in morphology and distribution in relation to cellular structures and the MnCO3 surface. For four fungi, Mn(II) oxidation occurred along hyphae, likely mediated by cell wall-associated proteins. For two species, Mn(II) oxidation occurred via reaction with fungal-derived superoxide produced at hyphal tips. This pathway ultimately resulted in structurally unique Mn oxide clusters formed at substantial distances from any cellular structure. Taken together, findings for these two fungi strongly point to a role for fungal-derived organic molecules in Mn(III) complexation and Mn oxide templation. Overall, this study illustrates the importance of fungi in rhodochrosite dissolution, extends the relevance of biogenic superoxide-based Mn(II) oxidation and highlights the potential role of mycogenic exudates in directing mineral precipitation.

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