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A Previously Uncharacterized, Nonphotosynthetic Member of the Chromatiaceae Is the Primary CO_2-Fixing Constituent in a Self-Regenerating Biocathode

Wang, Zheng and Leary, Dagmar H. and Malanoski, Anthony P. and Li, Robert W. and Hervey, W. Judson, IV and Eddie, Brian J. and Tender, Gabrielle S. and Yanosky, Shelley G. and Vora, Gary J. and Tender, Leonard M. and Lin, Baochuan and Strycharz-Glaven, Sarah M. (2015) A Previously Uncharacterized, Nonphotosynthetic Member of the Chromatiaceae Is the Primary CO_2-Fixing Constituent in a Self-Regenerating Biocathode. Applied and Environmental Microbiology, 81 (2). pp. 699-712. ISSN 0099-2240. PMCID PMC4277585.

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Biocathode extracellular electron transfer (EET) may be exploited for biotechnology applications, including microbially mediated O_2 reduction in microbial fuel cells and microbial electrosynthesis. However, biocathode mechanistic studies needed to improve or engineer functionality have been limited to a few select species that form sparse, homogeneous biofilms characterized by little or no growth. Attempts to cultivate isolates from biocathode environmental enrichments often fail due to a lack of some advantage provided by life in a consortium, highlighting the need to study and understand biocathode consortia in situ. Here, we present metagenomic and metaproteomic characterization of a previously described biocathode biofilm (+310 mV versus a standard hydrogen electrode [SHE]) enriched from seawater, reducing O_2, and presumably fixing CO_2 for biomass generation. Metagenomics identified 16 distinct cluster genomes, 15 of which could be assigned at the family or genus level and whose abundance was roughly divided between Alpha- and Gammaproteobacteria. A total of 644 proteins were identified from shotgun metaproteomics and have been deposited in the the ProteomeXchange with identifier PXD001045. Cluster genomes were used to assign the taxonomic identities of 599 proteins, with Marinobacter, Chromatiaceae, and Labrenzia the most represented. RubisCO and phosphoribulokinase, along with 9 other Calvin-Benson-Bassham cycle proteins, were identified from Chromatiaceae. In addition, proteins similar to those predicted for iron oxidation pathways of known iron-oxidizing bacteria were observed for Chromatiaceae. These findings represent the first description of putative EET and CO_2 fixation mechanisms for a self-regenerating, self-sustaining multispecies biocathode, providing potential targets for functional engineering, as well as new insights into biocathode EET pathways using proteomics.

Item Type:Article
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URLURL TypeDescription ItemSupplemetnal material
Malanoski, Anthony P.0000-0001-6192-888X
Eddie, Brian J.0000-0002-3559-3892
Tender, Leonard M.0000-0001-8784-991X
Alternate Title:A Previously Uncharacterized, Nonphotosynthetic Member of the Chromatiaceae Is the Primary CO2-Fixing Constituent in a Self-Regenerating Biocathode
Additional Information:© 2015, American Society for Microbiology. Received 9 September 2014 Accepted 5 November 2014. Accepted manuscript posted online 14 November 2014. Editor: A. M. Spormann. We thank the DoD High Performance Computing Modernization Program’s (HPCMP) PETTT staff at the Naval Research Laboratory for assistance with software configuration. We thank Martin Wu, University of Virginia, for assistance and guidance, particularly with the AMPHORA2 analysis. We also thank Daniel R. Bond, University of Minnesota, for helpful discussions regarding biocathode electron transfer. This work was funded by the Office of Naval Research via U.S. NRL core funds, as well as under the following award numbers (to S.M.S.-G.): N0001413WX20995, N0001414WX20485, and N0001414WX20518. The opinions and assertions contained here are ours and are not to be construed as those of the U.S. Navy, the military service at large, or the U.S. government.
Funding AgencyGrant Number
Office of Naval Research (ONR)N0001413WX20995
Office of Naval Research (ONR)N0001414WX20485
Office of Naval Research (ONR)N0001414WX20518
Issue or Number:2
PubMed Central ID:PMC4277585
Record Number:CaltechAUTHORS:20150206-102256272
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Official Citation:Wang Z, Leary DH, Malanoski AP, Li RW, Hervey WJ, IV, Eddie BJ, Tender GS, Yanosky SG, Vora GJ, Tender LM, Lin B, Strycharz-Glaven SM. 2015. A previously uncharacterized, nonphotosynthetic member of the Chromatiaceae is the primary CO2-fixing constituent in a self-regenerating biocathode. Appl Environ Microbiol 81:699 –712. doi:10.1128/AEM.02947-14.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:54476
Deposited By: Ruth Sustaita
Deposited On:06 Feb 2015 19:20
Last Modified:09 Mar 2020 13:19

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