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Title: Comparative Genomic Analysis of Neutrophilic Iron(II) Oxidizer Genomes for Candidate Genes in Extracellular Electron Transfer [Plus Supplementary Data]

Abstract

Extracellular electron transfer (EET) is recognized as a key biochemical process in circumneutral pH Fe(II)-oxidizing bacteria (FeOB). In this study, we searched for candidate EET genes in 73 neutrophilic FeOB genomes, among which 43 genomes are complete or close-to-complete and the rest have estimated genome completeness ranging from 5 to 91%. These neutrophilic FeOB span members of the microaerophilic, anaerobic phototrophic, and anaerobic nitrate-reducing FeOB groups. We found that many microaerophilic and several anaerobic FeOB possess homologs of Cyc2, an outer membrane cytochrome c originally identified in Acidithiobacillus ferrooxidans. The “porin-cytochrome c complex” (PCC) gene clusters homologous to MtoAB/PioAB are present in eight FeOB, accounting for 19% of complete and close-to-complete genomes examined, whereas PCC genes homologous to OmbB-OmaB-OmcB in Geobacter sulfurreducens are absent. Further, we discovered gene clusters that may potentially encode two novel PCC types. First, a cluster (tentatively named “PCC3”) encodes a porin, an extracellular and a periplasmic cytochrome c with remarkably large numbers of heme-binding motifs. Second, a cluster (tentatively named “PCC4”) encodes a porin and three periplasmic multiheme cytochromes c. A conserved inner membrane protein (IMP) encoded in PCC3 and PCC4 gene clusters might be responsible for translocating electrons across the inner membrane. Other bacteriamore » possessing PCC3 and PCC4 are mostly Proteobacteria isolated from environments with a potential niche for Fe(II) oxidation. In addition to cytochrome c, multicopper oxidase (MCO) genes potentially involved in Fe(II) oxidation were also identified. Notably, candidate EET genes were not found in some FeOB, especially the anaerobic ones, probably suggesting EET genes or Fe(II) oxidation mechanisms are different from the searched models. Overall, based on current EET models, the search extends our understanding of bacterial EET and provides candidate genes for future research.« less

Authors:
 [1];  [2];  [3];  [4]
  1. Univ. of Wisconsin, Madison, WI (United States). Dept. of Geoscience; Univ. of Wisconsin, Madison, WI (United States). NASA Astrobiology Institute; Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
  2. Bigelow Laboratory for Ocean Sciences, East Boothbay Harbor, ME (United States); Univ. of Southern California, Los Angeles, CA (United States). Dept. of Earth Sciences
  3. Bigelow Laboratory for Ocean Sciences, East Boothbay Harbor, ME (United States)
  4. Univ. of Wisconsin, Madison, WI (United States). Dept. of Geoscience; Univ. of Wisconsin, Madison, WI (United States). NASA Astrobiology Institute
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1628158
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; neutrophilic Fe(II) oxidation; extracellular electron transfer (EET); porin-cytochrome c complex (PCC); cytochrome c; multicopper oxidase; genomics

Citation Formats

He, Shaomei, Barco, Roman A., Emerson, David, and Roden, Eric E. Comparative Genomic Analysis of Neutrophilic Iron(II) Oxidizer Genomes for Candidate Genes in Extracellular Electron Transfer [Plus Supplementary Data]. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.01584.
He, Shaomei, Barco, Roman A., Emerson, David, & Roden, Eric E. Comparative Genomic Analysis of Neutrophilic Iron(II) Oxidizer Genomes for Candidate Genes in Extracellular Electron Transfer [Plus Supplementary Data]. United States. https://doi.org/10.3389/fmicb.2017.01584
He, Shaomei, Barco, Roman A., Emerson, David, and Roden, Eric E. Mon . "Comparative Genomic Analysis of Neutrophilic Iron(II) Oxidizer Genomes for Candidate Genes in Extracellular Electron Transfer [Plus Supplementary Data]". United States. https://doi.org/10.3389/fmicb.2017.01584. https://www.osti.gov/servlets/purl/1628158.
@article{osti_1628158,
title = {Comparative Genomic Analysis of Neutrophilic Iron(II) Oxidizer Genomes for Candidate Genes in Extracellular Electron Transfer [Plus Supplementary Data]},
author = {He, Shaomei and Barco, Roman A. and Emerson, David and Roden, Eric E.},
abstractNote = {Extracellular electron transfer (EET) is recognized as a key biochemical process in circumneutral pH Fe(II)-oxidizing bacteria (FeOB). In this study, we searched for candidate EET genes in 73 neutrophilic FeOB genomes, among which 43 genomes are complete or close-to-complete and the rest have estimated genome completeness ranging from 5 to 91%. These neutrophilic FeOB span members of the microaerophilic, anaerobic phototrophic, and anaerobic nitrate-reducing FeOB groups. We found that many microaerophilic and several anaerobic FeOB possess homologs of Cyc2, an outer membrane cytochrome c originally identified in Acidithiobacillus ferrooxidans. The “porin-cytochrome c complex” (PCC) gene clusters homologous to MtoAB/PioAB are present in eight FeOB, accounting for 19% of complete and close-to-complete genomes examined, whereas PCC genes homologous to OmbB-OmaB-OmcB in Geobacter sulfurreducens are absent. Further, we discovered gene clusters that may potentially encode two novel PCC types. First, a cluster (tentatively named “PCC3”) encodes a porin, an extracellular and a periplasmic cytochrome c with remarkably large numbers of heme-binding motifs. Second, a cluster (tentatively named “PCC4”) encodes a porin and three periplasmic multiheme cytochromes c. A conserved inner membrane protein (IMP) encoded in PCC3 and PCC4 gene clusters might be responsible for translocating electrons across the inner membrane. Other bacteria possessing PCC3 and PCC4 are mostly Proteobacteria isolated from environments with a potential niche for Fe(II) oxidation. In addition to cytochrome c, multicopper oxidase (MCO) genes potentially involved in Fe(II) oxidation were also identified. Notably, candidate EET genes were not found in some FeOB, especially the anaerobic ones, probably suggesting EET genes or Fe(II) oxidation mechanisms are different from the searched models. Overall, based on current EET models, the search extends our understanding of bacterial EET and provides candidate genes for future research.},
doi = {10.3389/fmicb.2017.01584},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Mon Aug 21 00:00:00 EDT 2017},
month = {Mon Aug 21 00:00:00 EDT 2017}
}

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Evidence for the biogenic origin of manganese-enriched layers in Lake Superior sediments: Biogenic origin of Mn-enriched sediment layers
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Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins
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The High-Molecular-Weight Cytochrome c Cyc2 of Acidithiobacillus ferrooxidans Is an Outer Membrane Protein
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Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics
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Fe-phyllosilicate redox cycling organisms from a redox transition zone in Hanford 300 Area sediments
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Comparative Genomic Insights into Ecophysiology of Neutrophilic, Microaerophilic Iron Oxidizing Bacteria
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The Role of FeOB in Engineered Water Ecosystems: A Review
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Physiological and Genomic Characterization of a Nitrate-Reducing Fe(II)-Oxidizing Bacterium Isolated from Paddy Soil
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