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Novel insights into the taxonomic diversity and molecular mechanisms of bacterial Mn(III) reduction

Nadia Szeinbaum, Brook L. Nunn, Amanda R. Cavazos, Sean A. Crowe, Frank J. Stewart, Thomas J. DiChristina, Christopher T. Reinhard, View ORCID ProfileJennifer B. Glass
doi: https://doi.org/10.1101/695007
Nadia Szeinbaum
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA
2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USA
6NASA Astrobiology Institute, Alternative Earths Team, Mountain View, CA
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Brook L. Nunn
3Department of Genome Sciences, University of Washington, Seattle, WA, USA
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Amanda R. Cavazos
2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USA
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Sean A. Crowe
2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USA
4Department of Microbiology & Immunology and Department of Earth, Ocean, & Atmospheric Sciences, University of British Columbia, Vancouver, Canada
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Frank J. Stewart
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA
5Department of Microbiology and Immunology, Montana State University, Bozeman, Montana
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Thomas J. DiChristina
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA
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Christopher T. Reinhard
2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USA
6NASA Astrobiology Institute, Alternative Earths Team, Mountain View, CA
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Jennifer B. Glass
2School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USA
6NASA Astrobiology Institute, Alternative Earths Team, Mountain View, CA
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  • ORCID record for Jennifer B. Glass
  • For correspondence: jennifer.glass@eas.gatech.edu
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Summary

Soluble ligand-bound Mn(III) can support anaerobic microbial respiration in diverse aquatic environments. Thus far, Mn(III) reduction has only been associated with certain Gammaproteobacteria. Here, we characterized microbial communities enriched from Mn-replete sediments of Lake Matano, Indonesia. Our results provide the first evidence for biological reduction of soluble Mn(III) outside the Gammaproteobacteria. Metagenome assembly and binning revealed a novel betaproteobacterium, which we designate “Candidatus Dechloromonas occultata.” This organism dominated the enrichment and expressed a porin-cytochrome c complex typically associated with iron-oxidizing Betaproteobacteria and a novel cytochrome c-rich protein cluster (Occ), including an undecaheme putatively involved in extracellular electron transfer. This occ gene cluster was also detected in diverse aquatic bacteria, including uncultivated Betaproteobacteria from the deep subsurface. These observations provide new insight into the taxonomic and functional diversity of microbially-driven Mn(III) reduction in natural environments.

Originality-Significance Statement Recent observations suggest that Mn(III)-ligand complexes are geochemically important in diverse aquatic environments. Thus far, microbially-driven Mn(III) reduction has only been associated with Gammaproteobacteria encoding three-component outer-membrane porin-cytochrome c conduits. Here, we demonstrate that Betaproteobacteria dominate in abundance and with respect to protein expression during biologically-mediated Mn(III) reduction in an enrichment culture from an anoxic lacustrine system. Using metaproteomics, we detect for the first time that Betaproteobacteria express a two-component porin-cytochrome c conduit, and an uncharacterized extracellular undecaheme (11-heme) c-type cytochrome. Although this is the first definitive report of an undecaheme within the Betaproteobacteria, we find evidence that they are widespread in uncultivated strains. These results widen the phylogenetic diversity of Mn(III)-reducing bacteria, and provide new insights into potential molecular mechanisms for soluble Mn(III) reduction

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • (1) commented on potential sources of contamination in the Mn(III) source (Supp. Information LL56-57); (2) further qualified uncertainties in the results and their relationship to methane oxidation; (3) clarified nitrogen chemistry discussion.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted June 27, 2020.
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Novel insights into the taxonomic diversity and molecular mechanisms of bacterial Mn(III) reduction
Nadia Szeinbaum, Brook L. Nunn, Amanda R. Cavazos, Sean A. Crowe, Frank J. Stewart, Thomas J. DiChristina, Christopher T. Reinhard, Jennifer B. Glass
bioRxiv 695007; doi: https://doi.org/10.1101/695007
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Novel insights into the taxonomic diversity and molecular mechanisms of bacterial Mn(III) reduction
Nadia Szeinbaum, Brook L. Nunn, Amanda R. Cavazos, Sean A. Crowe, Frank J. Stewart, Thomas J. DiChristina, Christopher T. Reinhard, Jennifer B. Glass
bioRxiv 695007; doi: https://doi.org/10.1101/695007

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