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 »
- Authors:
-
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Univ. of Minnesota, St. Paul, MN (United States). Dept. of Microbiology
- Univ. of East Anglia, Norwich (United Kingdom). Center for Molecular and Structural Biochemistry, School of Biological Sciences and School of Chemistry
- Washington State Univ., Pullman, WA (United States). Gene and Linda Voiland School of Chemical Engineering and Bioengineering
- 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}
}
Web of Science
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Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners
journal, April 2018
- Edwards, Marcus J.; White, Gaye F.; Lockwood, Colin W.
- Journal of Biological Chemistry, Vol. 293, Issue 21
Possibilities for extremophilic microorganisms in microbial electrochemical systems
journal, October 2015
- Dopson, Mark; Ni, Gaofeng; Sleutels, Tom HJA
- FEMS Microbiology Reviews, Vol. 40, Issue 2
Genome Scale Mutational Analysis of Geobacter sulfurreducens Reveals Distinct Molecular Mechanisms for Respiration and Sensing of Poised Electrodes versus Fe(III) Oxides
journal, July 2017
- Chan, Chi Ho; Levar, Caleb E.; Jiménez-Otero, Fernanda
- Journal of Bacteriology, Vol. 199, Issue 19
Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes
journal, September 2017
- He, Shaomei; Stevens, Sarah L. R.; Chan, Leong-Keat
- mSphere, Vol. 2, Issue 5
Genomic analyses of bacterial porin-cytochrome gene clusters
journal, November 2014
- Shi, Liang; Fredrickson, James K.; Zachara, John M.
- Frontiers in Microbiology, Vol. 5
Rational engineering of Geobacter sulfurreducens electron transfer components: a foundation for building improved Geobacter-based bioelectrochemical technologies
journal, July 2015
- Dantas, Joana M.; Morgado, Leonor; Aklujkar, Muktak
- Frontiers in Microbiology, Vol. 6
Comparative Proteomic Analysis of Desulfotomaculum reducens MI-1: Insights into the Metabolic Versatility of a Gram-Positive Sulfate- and Metal-Reducing Bacterium
journal, February 2016
- Otwell, Anne E.; Callister, Stephen J.; Zink, Erika M.
- Frontiers in Microbiology, Vol. 7
Comparative Genomic Analysis of Neutrophilic Iron(II) Oxidizer Genomes for Candidate Genes in Extracellular Electron Transfer
journal, August 2017
- He, Shaomei; Barco, Roman A.; Emerson, David
- Frontiers in Microbiology, Vol. 8
Genomic Analyses of the Quinol Oxidases and/or Quinone Reductases Involved in Bacterial Extracellular Electron Transfer
journal, December 2018
- Zhong, Yuhong; Shi, Liang
- Frontiers in Microbiology, Vol. 9
Bespoke Biomolecular Wires for Transmembrane Electron Transfer: Spontaneous Assembly of a Functionalized Multiheme Electron Conduit
journal, August 2021
- Piper, Samuel E. H.; Edwards, Marcus J.; van Wonderen, Jessica H.
- Frontiers in Microbiology, Vol. 12
Characterization of a Novel Porin-Like Protein, ExtI, from Geobacter sulfurreducens and Its Implication in the Reduction of Selenite and Tellurite
journal, March 2018
- Jahan, Mst. Ishrat; Tobe, Ryuta; Mihara, Hisaaki
- International Journal of Molecular Sciences, Vol. 19, Issue 3