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

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

doi:10.1111/1758-2229.12204

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

Journal Article · Wed Sep 24 00:00:00 EDT 2014 · Environmental Microbiology Reports

DOI:https://doi.org/10.1111/1758-2229.12204· OSTI ID:1167625

Liu, Yimo ^[1]; Wang, Zheming ^[1]; Liu, Juan ^[1]; Levar, Caleb ^[2]; Edwards, Marcus ^[3]; Babauta, Jerome T. ^[4]; Kennedy, David W. ^[1]; Shi, Zhi ^[1]; Beyenal, Haluk ^[4]; Bond, Daniel R. ^[2]; Clarke, Thomas A. ^[5]; Butt, Julea N. ^[5]; Richardson, David J. ^[5]; Rosso, Kevin M. ^[1]; Zachara, John M. ^[1]; Fredrickson, Jim K. ^[1]; Shi, Liang ^[1]

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

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830; SC0007229

OSTI ID:: 1167625

Report Number(s):: PNNL-SA-104799; KP1702030

Journal Information:: Environmental Microbiology Reports, Vol. 6, Issue 6; ISSN 1758-2229

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 131 works

Citation information provided by
Web of Science

References (47)

The X-ray crystal structure of Shewanella oneidensis OmcA reveals new insight at the microbe-mineral interface Edwards, Marcus J.; Baiden, Nanakow A.; Johs, Alexander FEBS Letters, Vol. 588, Issue 10 https://doi.org/10.1016/j.febslet.2014.04.013	journal	April 2014
OmcB, a c-Type Polyheme Cytochrome, Involved in Fe(III) Reduction in Geobacter sulfurreducens Leang, C.; Coppi, M. V.; Lovley, D. R. Journal of Bacteriology, Vol. 185, Issue 7 https://doi.org/10.1128/JB.185.7.2096-2103.2003	journal	April 2003
Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens Mehta, T.; Coppi, M. V.; Childers, S. E. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8634-8641.2005	journal	December 2005
Adaptation to Disruption of the Electron Transfer Pathway for Fe(III) Reduction in Geobacter sulfurreducens Leang, C.; Adams, L. A.; Chin, K. -J. Journal of Bacteriology, Vol. 187, Issue 17 https://doi.org/10.1128/JB.187.17.5918-5926.2005	journal	August 2005
Ferrozine---a new spectrophotometric reagent for iron Stookey, Lawrence L. Analytical Chemistry, Vol. 42, Issue 7, p. 779-781 https://doi.org/10.1021/ac60289a016	journal	June 1970
Structure of the Type IVa Major Pilin from the Electrically Conductive Bacterial Nanowires of Geobacter sulfurreducens Reardon, Patrick N.; Mueller, Karl T. Journal of Biological Chemistry, Vol. 288, Issue 41 https://doi.org/10.1074/jbc.M113.498527	journal	August 2013
Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals White, G. F.; Shi, Z.; Shi, L. Proceedings of the National Academy of Sciences, Vol. 110, Issue 16 https://doi.org/10.1073/pnas.1220074110	journal	March 2013
Tunable metallic-like conductivity in microbial nanowire networks Malvankar, Nikhil S.; Vargas, Madeline; Nevin, Kelly P. Nature Nanotechnology, Vol. 6, Issue 9 https://doi.org/10.1038/nnano.2011.119	journal	August 2011
Structure of a bacterial cell surface decaheme electron conduit Clarke, T. A.; Edwards, M. J.; Gates, A. J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 23 https://doi.org/10.1073/pnas.1017200108	journal	May 2011
Regulation of two highly similar genes, omcB and omcC, in a 10 kb chromosomal duplication in Geobacter sulfurreducens Leang, C. Microbiology, Vol. 151, Issue 6 https://doi.org/10.1099/mic.0.27870-0	journal	June 2005
Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes Butler, Jessica E.; Young, Nelson D.; Lovley, Derek R. BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-40	journal	January 2010
Aromatic Amino Acids Required for Pili Conductivity and Long-Range Extracellular Electron Transport in Geobacter sulfurreducens Vargas, Madeline; Malvankar, Nikhil S.; Tremblay, Pier-Luc mBio, Vol. 4, Issue 2 https://doi.org/10.1128/mBio.00210-13	journal	April 2013
Mtr extracellular electron-transfer pathways in Fe(III)-reducing or Fe(II)-oxidizing bacteria: a genomic perspective Shi, Liang; Rosso, Kevin M.; Zachara, John M. Biochemical Society Transactions, Vol. 40, Issue 6 https://doi.org/10.1042/BST20120098	journal	November 2012
Development of a Genetic System for Geobacter sulfurreducens Coppi, M. V.; Leang, C.; Sandler, S. J. Applied and Environmental Microbiology, Vol. 67, Issue 7, p. 3180-3187 https://doi.org/10.1128/AEM.67.7.3180-3187.2001	journal	July 2001
The Crystal Structure of the Extracellular 11-heme Cytochrome UndA Reveals a Conserved 10-heme Motif and Defined Binding Site for Soluble Iron Chelates Edwards, Marcus J.; Hall, Andrea; Shi, Liang Structure, Vol. 20, Issue 7 https://doi.org/10.1016/j.str.2012.04.016	journal	July 2012
Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens Qian, Xinlei; Mester, Tünde; Morgado, Leonor Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 4 https://doi.org/10.1016/j.bbabio.2011.01.003	journal	April 2011
In-gel digestion for mass spectrometric characterization of proteins and proteomes Shevchenko, Andrej; Tomas, Henrik; Havli, Jan Nature Protocols, Vol. 1, Issue 6 https://doi.org/10.1038/nprot.2006.468	journal	December 2006
Isolation of a High-Affinity Functional Protein Complex between OmcA and MtrC: Two Outer Membrane Decaheme c-Type Cytochromes of Shewanella oneidensis MR-1 Shi, L.; Chen, B.; Wang, Z. Journal of Bacteriology, Vol. 188, Issue 13 https://doi.org/10.1128/JB.01966-05	journal	June 2006
Towards environmental systems biology of Shewanella Fredrickson, James K.; Romine, Margaret F.; Beliaev, Alexander S. Nature Reviews Microbiology, Vol. 6, Issue 8 https://doi.org/10.1038/nrmicro1947	journal	July 2008
Extracellular electron transfer via microbial nanowires Reguera, Gemma; McCarthy, Kevin D.; Mehta, Teena Nature, Vol. 435, Issue 7045, p. 1098-1101 https://doi.org/10.1038/nature03661	journal	June 2005
Direct Involvement of Type II Secretion System in Extracellular Translocation of Shewanella oneidensis Outer Membrane Cytochromes MtrC and OmcA Shi, L.; Deng, S.; Marshall, M. J. Journal of Bacteriology, Vol. 190, Issue 15 https://doi.org/10.1128/JB.00514-08	journal	May 2008
Identification and Characterization of MtoA: A Decaheme c-Type Cytochrome of the Neutrophilic Fe(II)-Oxidizing Bacterium Sideroxydans lithotrophicus ES-1 Liu, Juan; Wang, Zheming; Belchik, Sara M. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00037	journal	January 2012
The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions Ding, Yan-Huai R.; Hixson, Kim K.; Giometti, Carol S. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1764, Issue 7 https://doi.org/10.1016/j.bbapap.2006.04.017	journal	July 2006
Bug juice: harvesting electricity with microorganisms Lovley, Derek R. Nature Reviews Microbiology, Vol. 4, Issue 7, p. 497-508 https://doi.org/10.1038/nrmicro1442	journal	July 2006
Alignment of the c-Type Cytochrome OmcS along Pili of Geobacter sulfurreducens Leang, C.; Qian, X.; Mester, T. Applied and Environmental Microbiology, Vol. 76, Issue 12, p. 4080-4084 https://doi.org/10.1128/AEM.00023-10	journal	April 2010
A putative multicopper protein secreted by an atypical type II secretion system involved in the reduction of insoluble electron acceptors in Geobacter sulfurreducens Mehta, T. Microbiology, Vol. 152, Issue 8 https://doi.org/10.1099/mic.0.28864-0	journal	August 2006
Antibody Recognition Force Microscopy Shows that Outer Membrane Cytochromes OmcA and MtrC Are Expressed on the Exterior Surface of Shewanella oneidensis MR-1 Lower, B. H.; Yongsunthon, R.; Shi, L. Applied and Environmental Microbiology, Vol. 75, Issue 9 https://doi.org/10.1128/AEM.02108-08	journal	March 2009
Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones Okamoto, A.; Hashimoto, K.; Nealson, K. H. Proceedings of the National Academy of Sciences, Vol. 110, Issue 19 https://doi.org/10.1073/pnas.1220823110	journal	April 2013
Respiration of metal (hydr)oxides by Shewanella and Geobacter : a key role for multihaem c -type cytochromes Shi, Liang; Squier, Thomas C.; Zachara, John M. Molecular Microbiology, Vol. 65, Issue 1 https://doi.org/10.1111/j.1365-2958.2007.05783.x	journal	July 2007
Characterization of an electron conduit between bacteria and the extracellular environment Hartshorne, Robert S.; Reardon, Catherine L.; Ross, Daniel Proceedings of the National Academy of Sciences, Vol. 106, Issue 52 https://doi.org/10.1073/pnas.0900086106	journal	December 2009
The ‘porin-cytochrome’ model for microbe-to-mineral electron transfer: Microbe-to-mineral electron transfer Richardson, David J.; Butt, Julea N.; Fredrickson, Jim K. Molecular Microbiology, Vol. 85, Issue 2 https://doi.org/10.1111/j.1365-2958.2012.08088.x	journal	May 2012
Characterization of Protein-Protein Interactions Involved in Iron Reduction by Shewanella oneidensis MR-1 Ross, D. E.; Ruebush, S. S.; Brantley, S. L. Applied and Environmental Microbiology, Vol. 73, Issue 18 https://doi.org/10.1128/AEM.00146-07	journal	August 2007
Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics Emerson, David; Field, Erin K.; Chertkov, Olga Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00254	journal	January 2013
Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins Qian, Xinlei; Reguera, Gemma; Mester, TÃ¼nde FEMS Microbiology Letters, Vol. 277, Issue 1 https://doi.org/10.1111/j.1574-6968.2007.00915.x	journal	December 2007
Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction Weber, Karrie A.; Achenbach, Laurie A.; Coates, John D. Nature Reviews Microbiology, Vol. 4, Issue 10, p. 752-764 https://doi.org/10.1038/nrmicro1490	journal	October 2006
Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens Aklujkar, M.; Coppi, M. V.; Leang, C. Microbiology, Vol. 159, Issue Pt_3 https://doi.org/10.1099/mic.0.064089-0	journal	January 2013
Iron Oxides in the Laboratary Schwertmann, U.; Cornell, R. M. WILEY-VCH Verlag GmbH https://doi.org/10.1002/9783527613229	book	April 2000
Bioenergetic challenges of microbial iron metabolisms Bird, Lina J.; Bonnefoy, Violaine; Newman, Dianne K. Trends in Microbiology, Vol. 19, Issue 7 https://doi.org/10.1016/j.tim.2011.05.001	journal	July 2011
Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens Lloyd, Jon R.; Leang, Ching; Myerson, Allison L. HODGES Biochemical Journal, Vol. 369, Issue 1 https://doi.org/10.1042/bj20020597	journal	January 2003
PRED-TMBB: a web server for predicting the topology of -barrel outer membrane proteins Bagos, P. G.; Liakopoulos, T. D.; Spyropoulos, I. C. Nucleic Acids Research, Vol. 32, Issue Web Server https://doi.org/10.1093/nar/gkh417	journal	July 2004
Genes for two multicopper proteins required for Fe(III) oxide reduction in Geobacter sulfurreducens have different expression patterns both in the subsurface and on energy-harvesting electrodes Holmes, D. E.; Mester, T.; O'Neil, R. A. Microbiology, Vol. 154, Issue 5 https://doi.org/10.1099/mic.0.2007/014365-0	journal	May 2008
The pio Operon Is Essential for Phototrophic Fe(II) Oxidation in Rhodopseudomonas palustris TIE-1 Jiao, Y.; Newman, D. K. Journal of Bacteriology, Vol. 189, Issue 5 https://doi.org/10.1128/JB.00776-06	journal	December 2006
Structure of the Type IVa Major Pilin from the Electrically Conductive Bacterial Nanowires of Geobacter sulfurreducens Reardon, Patrick N.; Mueller, Karl T. Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr19185	dataset	January 2013
Enzyme or Electrode? Einsle, Oliver Structure, Vol. 20, Issue 7 https://doi.org/10.1016/j.str.2012.06.005	journal	July 2012
The crystal structure of the pentahaem c-type cytochrome NrfB and characterization of its solution-state interaction with the pentahaem nitrite reductase NrfA Clarke, Thomas A.; Cole, Jeffrey A.; Richardson, David J. Biochemical Journal, Vol. 406, Issue 1 https://doi.org/10.1042/bj20070321	journal	July 2007
Development of a proteoliposome model to probe transmembrane electron-transfer reactions White, Gaye F.; Shi, Zhi; Shi, Liang Biochemical Society Transactions, Vol. 40, Issue 6 https://doi.org/10.1042/bst20120116	journal	November 2012
Identification of Genes Involved in Biofilm Formation and Respiration via Mini-Himar Transposon Mutagenesis of Geobacter sulfurreducens Rollefson, J. B.; Levar, C. E.; Bond, D. R. Journal of Bacteriology, Vol. 191, Issue 13 https://doi.org/10.1128/jb.00057-09	journal	April 2009

Cited By (26)

Role of multiheme cytochromes involved in extracellular anaerobic respiration in bacteria Edwards, Marcus J.; Richardson, David J.; Paquete, Catarina M. Protein Science, Vol. 29, Issue 4 https://doi.org/10.1002/pro.3787	journal	November 2019
A review of the mechanisms of mineral-based metabolism in early Earth analog rock-hosted hydrothermal ecosystems Amenabar, Maximiliano J.; Boyd, Eric S. World Journal of Microbiology and Biotechnology, Vol. 35, Issue 2 https://doi.org/10.1007/s11274-019-2604-2	journal	January 2019
Molecular underpinnings for microbial extracellular electron transfer during biogeochemical cycling of earth elements Jiang, Yongguang; Shi, Meimei; Shi, Liang Science China Life Sciences, Vol. 62, Issue 10 https://doi.org/10.1007/s11427-018-9464-3	journal	March 2019
Enhanced microbial electrosynthesis by using defined co-cultures Deutzmann, Jörg S.; Spormann, Alfred M. The ISME Journal, Vol. 11, Issue 3 https://doi.org/10.1038/ismej.2016.149	journal	November 2016
Chemolithotrophic processes in the bacterial communities on the surface of mineral-enriched biochars Ye, Jun; Joseph, Stephen D.; Ji, Mukan The ISME Journal, Vol. 11, Issue 5 https://doi.org/10.1038/ismej.2016.187	journal	February 2017
Syntrophic anaerobic photosynthesis via direct interspecies electron transfer Ha, Phuc T.; Lindemann, Stephen R.; Shi, Liang Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms13924	journal	January 2017
Extracellular electron transfer mechanisms between microorganisms and minerals Shi, Liang; Dong, Hailiang; Reguera, Gemma Nature Reviews Microbiology, Vol. 14, Issue 10 https://doi.org/10.1038/nrmicro.2016.93	journal	August 2016
Comparative metatranscriptomics reveals extracellular electron transfer pathways conferring microbial adaptivity to surface redox potential changes Ishii, Shun’ichi; Suzuki, Shino; Tenney, Aaron The ISME Journal, Vol. 12, Issue 12 https://doi.org/10.1038/s41396-018-0238-2	journal	July 2018
Application of electrochemical surface plasmon resonance (ESPR) to the study of electroactive microbial biofilms Golden, Joel; Yates, Matthew D.; Halsted, Michelle Physical Chemistry Chemical Physics, Vol. 20, Issue 40 https://doi.org/10.1039/c8cp03898h	journal	January 2018
A review on the biosynthesis of metal and metal salt nanoparticles by microbes Gahlawat, Geeta; Choudhury, Anirban Roy RSC Advances, Vol. 9, Issue 23 https://doi.org/10.1039/c8ra10483b	journal	January 2019
Interaction studies between periplasmic cytochromes provide insights into extracellular electron transfer pathways of Geobacter sulfurreducens Fernandes, Ana P.; Nunes, Tiago C.; Paquete, Catarina M. Biochemical Journal, Vol. 474, Issue 5 https://doi.org/10.1042/bcj20161022	journal	February 2017
Redox-gradient driven electron transport in a mixed community anodic biofilm Yates, Matthew D.; Barr Engel, Sarah; Eddie, Brian J. FEMS Microbiology Ecology, Vol. 94, Issue 6 https://doi.org/10.1093/femsec/fiy081	journal	May 2018
Microbial nanowires and electroactive biofilms Reguera, Gemma FEMS Microbiology Ecology, Vol. 94, Issue 7 https://doi.org/10.1093/femsec/fiy086	journal	May 2018
Genomes of ubiquitous marine and hypersaline Hydrogenovibrio , Thiomicrorhabdus and Thiomicrospira spp. encode a diversity of mechanisms to sustain chemolithoautotrophy in heterogeneous environments : Hydrogenovibrio, Thiomicrorhabdus, Thiomicrospira Scott, Kathleen M.; Williams, John; Porter, Cody M. B. Environmental Microbiology, Vol. 20, Issue 8 https://doi.org/10.1111/1462-2920.14090	journal	April 2018
Electromicrobiology: realities, grand challenges, goals and predictions Nealson, Kenneth H.; Rowe, Annette R. Microbial Biotechnology, Vol. 9, Issue 5 https://doi.org/10.1111/1751-7915.12400	journal	August 2016
Isolation and Characterization of a Novel Electrogenic Bacterium, Dietzia sp. RNV-4 Sacco, Natalia J.; Bonetto, M. Celina; Cortón, Eduardo PLOS ONE, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pone.0169955	journal	February 2017
Rational engineering of Geobacter sulfurreducens electron transfer components: a foundation for building improved Geobacter-based bioelectrochemical technologies Dantas, Joana M.; Morgado, Leonor; Aklujkar, Muktak Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00752	journal	July 2015
Comparative Genomic Analysis of Neutrophilic Iron(II) Oxidizer Genomes for Candidate Genes in Extracellular Electron Transfer He, Shaomei; Barco, Roman A.; Emerson, David Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01584	journal	August 2017
A unique aromatic residue modulates the redox range of a periplasmic multiheme cytochrome from Geobacter metallireducens Portela, Pilar C.; Silva, Marta A.; Teixeira, Liliana R. Journal of Biological Chemistry, Vol. 296 https://doi.org/10.1016/j.jbc.2021.100711	journal	January 2021
Possibilities for extremophilic microorganisms in microbial electrochemical systems Dopson, Mark; Ni, Gaofeng; Sleutels, Tom HJA FEMS Microbiology Reviews, Vol. 40, Issue 2 https://doi.org/10.1093/femsre/fuv044	journal	October 2015
Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes He, Shaomei; Stevens, Sarah L. R.; Chan, Leong-Keat mSphere, Vol. 2, Issue 5 https://doi.org/10.1128/msphere.00277-17	journal	September 2017
Genomic analyses of bacterial porin-cytochrome gene clusters Shi, Liang; Fredrickson, James K.; Zachara, John M. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00657	journal	November 2014
Comparative Proteomic Analysis of Desulfotomaculum reducens MI-1: Insights into the Metabolic Versatility of a Gram-Positive Sulfate- and Metal-Reducing Bacterium Otwell, Anne E.; Callister, Stephen J.; Zink, Erika M. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00191	journal	February 2016
Genomic Analyses of the Quinol Oxidases and/or Quinone Reductases Involved in Bacterial Extracellular Electron Transfer Zhong, Yuhong; Shi, Liang Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03029	journal	December 2018
Bespoke Biomolecular Wires for Transmembrane Electron Transfer: Spontaneous Assembly of a Functionalized Multiheme Electron Conduit Piper, Samuel E. H.; Edwards, Marcus J.; van Wonderen, Jessica H. Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.714508	journal	August 2021
Characterization of a Novel Porin-Like Protein, ExtI, from Geobacter sulfurreducens and Its Implication in the Reduction of Selenite and Tellurite Jahan, Mst. Ishrat; Tobe, Ryuta; Mihara, Hisaaki International Journal of Molecular Sciences, Vol. 19, Issue 3 https://doi.org/10.3390/ijms19030809	journal	March 2018

Similar Records

Direct involvement of ombB, omaB, and omcB genes in extracellular reduction of Fe(III) by Geobacter sulfurreducens PCA

Journal Article · Thu Oct 01 00:00:00 EDT 2015 · Frontiers in Microbiology · OSTI ID:1167625

Liu, Yimo; Fredrickson, Jim K.; Zachara, John M.; +1 more

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

Journal Article · Mon Aug 21 00:00:00 EDT 2017 · Frontiers in Microbiology · OSTI ID:1167625

He, Shaomei; Barco, Roman A.; Emerson, David; +1 more

Genomic analyses of bacterial porin-cytochrome gene clusters

Journal Article · Wed Nov 26 00:00:00 EST 2014 · Frontiers in Microbiology · OSTI ID:1167625

Shi, Liang; Fredrickson, James K.; Zachara, John M.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
element cycles and biogeochemical processes
metals
bacteria

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

Citation Formats

References (47)

Cited By (26)

Similar Records

Related Subjects