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Title: A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA

Abstract

The multiheme, outer membrane c-type cytochrome (c-Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across the outer membrane. However, the underlying mechanism has remained uncharacterized. In G. sulfurreducens, the omcB gene is part of two tandem four-gene clusters, each is predicted to encode a transcriptional factor (OrfR/OrfS), a porin-like outer membrane protein (OmbB/OmbC), a periplasmic c-type cytochrome (OmaB/OmaC), and an outer membrane c-Cyt (OmcB/OmcC), respectively. Here we showed that OmbB/OmbC, OmaB/OmaC and OmcB/OmcC of G. sulfurreducens PCA formed the porin-cytochrome (Pcc) protein complexes, which were involved in transferring electrons across the outer membrane. The isolated Pcc protein complexes reconstituted in proteoliposomes transferred electrons from reduced methyl viologen across the lipid bilayer of liposomes to Fe(III)-citrate and ferrihydrite. The pcc clusters were found in all eight sequenced Geobacter and 11 other bacterial genomes from six different phyla, demonstrating a widespread distribution of Pcc protein complexes in phylogenetically diverse bacteria. Deletion of ombB-omaB-omcB-orfS-ombC-omaC-omcC gene clusters had no impact on the growth of G. sulfurreducens PCA with fumarate, but diminished the ability of G. sulfurreducens PCA to reduce Fe(III)-citrate and ferrihydrite. Finally, complementation with the ombB-omaB-omcB gene cluster restored the ability of G. sulfurreducens PCA to reduce Fe(III)-citrate andmore » ferrihydrite.« less

Authors:
 [1];  [1];  [1];  [2];  [3];  [4];  [1];  [1];  [4];  [2];  [5];  [5];  [5];  [1];  [1];  [1];  [1]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  2. Univ. of Minnesota, St. Paul, MN (United States). Dept. of Microbiology
  3. Univ. of East Anglia, Norwich (United Kingdom). Center for Molecular and Structural Biochemistry, School of Biological Sciences and School of Chemistry
  4. Washington State Univ., Pullman, WA (United States). Gene and Linda Voiland School of Chemical Engineering and Bioengineering
  5. Univ. of East Anglia, Norwich (United Kingdom). Center for Molecular and Structural Biochemistry, School of Biological Sciences and School of Chemistry
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1167625
Report Number(s):
PNNL-SA-104799
Journal ID: ISSN 1758-2229; KP1702030
Grant/Contract Number:  
AC05-76RL01830; SC0007229
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology Reports
Additional Journal Information:
Journal Volume: 6; Journal Issue: 6; Journal ID: ISSN 1758-2229
Publisher:
Wiley-Blackwell
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; element cycles and biogeochemical processes; metals; bacteria

Citation Formats

Liu, Yimo, Wang, Zheming, Liu, Juan, Levar, Caleb, Edwards, Marcus, Babauta, Jerome T., Kennedy, David W., Shi, Zhi, Beyenal, Haluk, Bond, Daniel R., Clarke, Thomas A., Butt, Julea N., Richardson, David J., Rosso, Kevin M., Zachara, John M., Fredrickson, Jim K., and Shi, Liang. A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA. United States: N. p., 2014. Web. doi:10.1111/1758-2229.12204.
Liu, Yimo, Wang, Zheming, Liu, Juan, Levar, Caleb, Edwards, Marcus, Babauta, Jerome T., Kennedy, David W., Shi, Zhi, Beyenal, Haluk, Bond, Daniel R., Clarke, Thomas A., Butt, Julea N., Richardson, David J., Rosso, Kevin M., Zachara, John M., Fredrickson, Jim K., & Shi, Liang. A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA. United States. https://doi.org/10.1111/1758-2229.12204
Liu, Yimo, Wang, Zheming, Liu, Juan, Levar, Caleb, Edwards, Marcus, Babauta, Jerome T., Kennedy, David W., Shi, Zhi, Beyenal, Haluk, Bond, Daniel R., Clarke, Thomas A., Butt, Julea N., Richardson, David J., Rosso, Kevin M., Zachara, John M., Fredrickson, Jim K., and Shi, Liang. Wed . "A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA". United States. https://doi.org/10.1111/1758-2229.12204. https://www.osti.gov/servlets/purl/1167625.
@article{osti_1167625,
title = {A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA},
author = {Liu, Yimo and Wang, Zheming and Liu, Juan and Levar, Caleb and Edwards, Marcus and Babauta, Jerome T. and Kennedy, David W. and Shi, Zhi and Beyenal, Haluk and Bond, Daniel R. and Clarke, Thomas A. and Butt, Julea N. and Richardson, David J. and Rosso, Kevin M. and Zachara, John M. and Fredrickson, Jim K. and Shi, Liang},
abstractNote = {The multiheme, outer membrane c-type cytochrome (c-Cyt) OmcB of Geobacter sulfurreducens was previously proposed to mediate electron transfer across the outer membrane. However, the underlying mechanism has remained uncharacterized. In G. sulfurreducens, the omcB gene is part of two tandem four-gene clusters, each is predicted to encode a transcriptional factor (OrfR/OrfS), a porin-like outer membrane protein (OmbB/OmbC), a periplasmic c-type cytochrome (OmaB/OmaC), and an outer membrane c-Cyt (OmcB/OmcC), respectively. Here we showed that OmbB/OmbC, OmaB/OmaC and OmcB/OmcC of G. sulfurreducens PCA formed the porin-cytochrome (Pcc) protein complexes, which were involved in transferring electrons across the outer membrane. The isolated Pcc protein complexes reconstituted in proteoliposomes transferred electrons from reduced methyl viologen across the lipid bilayer of liposomes to Fe(III)-citrate and ferrihydrite. The pcc clusters were found in all eight sequenced Geobacter and 11 other bacterial genomes from six different phyla, demonstrating a widespread distribution of Pcc protein complexes in phylogenetically diverse bacteria. Deletion of ombB-omaB-omcB-orfS-ombC-omaC-omcC gene clusters had no impact on the growth of G. sulfurreducens PCA with fumarate, but diminished the ability of G. sulfurreducens PCA to reduce Fe(III)-citrate and ferrihydrite. Finally, complementation with the ombB-omaB-omcB gene cluster restored the ability of G. sulfurreducens PCA to reduce Fe(III)-citrate and ferrihydrite.},
doi = {10.1111/1758-2229.12204},
journal = {Environmental Microbiology Reports},
number = 6,
volume = 6,
place = {United States},
year = {Wed Sep 24 00:00:00 EDT 2014},
month = {Wed Sep 24 00:00:00 EDT 2014}
}

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