Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Electron transport across the cell envelope via multiheme c-type cytochromes in Geobacter sulfurreducens

Journal Article · · Frontiers in Chemistry
 [1];  [1]
  1. University of California, Irvine, CA (United States)
Extracellular electron transfer (EET) enables certain microorganisms to respire using soluble and insoluble extracellular electron acceptors by transporting electrons across the cell envelope. Among these, G. sulfurreducens serves as a model organism for understanding direct EET pathways, where multiheme c-type cytochromes mediate electron transport from intracellular redox carriers to extracellular acceptors such as Fe(III) oxides and electrodes. This review focuses on heme-dependent electron transfer in Geobacter sulfurreducens, detailing the roles of inner membrane cytochromes, periplasmic carriers, outer membrane conduits, and recently characterized extracellular nanowires formed by polymerized multiheme c-type cytochromes, including OmcS, OmcE, and OmcZ. We examine the state of understanding of their physiological function, their structural features, expression patterns, and essentiality under various respiratory conditions. These insights advance our understanding of microbial anaerobic respiration and have implications for biogeochemical cycling, bioenergy generation, and bioremediation. The molecular architecture, assembly mechanisms, and secretion pathways of multiheme c-type cytochrome nanowires remain active areas of investigation, offering promising directions for future research and biotechnological innovation in engineered microbial systems.
Research Organization:
University of California, Irvine, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0020322
OSTI ID:
3003913
Journal Information:
Frontiers in Chemistry, Journal Name: Frontiers in Chemistry Vol. 13; ISSN 2296-2646
Publisher:
Frontiers Media SACopyright Statement
Country of Publication:
United States
Language:
English

References (91)

Real-Time Spatial Gene Expression Analysis within Current-Producing Biofilms journal May 2012
On Electron Transport through Geobacter Biofilms journal May 2012
Geobacter sulfurreducens metabolism at different donor/acceptor ratios journal September 2022
Characterization of the inner membrane cytochrome ImcH from Geobacter reveals its importance for extracellular electron transfer and energy conservation journal October 2023
Periplasmic electron transfer network in Geobacter sulfurreducens revealed by biomolecular interaction studies journal June 2024
Tethered heme domains in a triheme cytochrome allow for increased electron transport distances journal October 2024
Bacterial reduction of hexavalent chromium journal February 1995
Oxidation of acetate through reactions of the citric acid cycle by Geobacter sulfurreducens in pure culture and in syntrophic coculture journal November 2000
Bioremediation of metal contamination journal June 1997
The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions journal July 2006
Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or Fe(III) citrate as the electron acceptor journal December 2008
Reduction of low potential electron acceptors requires the CbcL inner membrane cytochrome of Geobacter sulfurreducens journal February 2016
The blind men and the filament: Understanding structures and functions of microbial nanowires journal December 2020
Extracellular electron transfer (EET) enhanced anammox process for progressive nitrogen removal: A review journal February 2024
Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers journal April 2019
Extracellular cytochrome nanowires appear to be ubiquitous in prokaryotes journal June 2023
A widespread and ancient bacterial machinery assembles cytochrome OmcS nanowires essential for extracellular electron transfer journal February 2025
Hemes on a string: insights on the functional mechanisms of PgcA from Geobacter sulfurreducens journal October 2023
Extracellular Electron Uptake: Among Autotrophs and Mediated by Surfaces journal April 2017
Microbial nanowires: type IV pili or cytochrome filaments? journal April 2023
Redox potential as a master variable controlling pathways of metal reduction by Geobacter sulfurreducens journal January 2017
Extracellular electron transfer via microbial nanowires journal June 2005
Tunable metallic-like conductivity in microbial nanowire networks journal August 2011
Measuring conductivity of living Geobacter sulfurreducens biofilms journal November 2016
Extracellular electron transfer mechanisms between microorganisms and minerals journal August 2016
Exoelectrogenic bacteria that power microbial fuel cells journal March 2009
Syntrophic growth with direct interspecies electron transfer between pili-free Geobacter species journal June 2018
Microbial biofilms as living photoconductors due to ultrafast electron transfer in cytochrome OmcS nanowires journal September 2022
Widespread extracellular electron transfer pathways for charging microbial cytochrome OmcS nanowires via periplasmic cytochromes PpcABCDE journal March 2024
Cryo-EM structure of an extracellular Geobacter OmcE cytochrome filament reveals tetrahaem packing journal July 2022
Structure of Geobacter cytochrome OmcZ identifies mechanism of nanowire assembly and conductivity journal February 2023
Electroactive microorganisms in bioelectrochemical systems journal March 2019
Power generation from ambient humidity using protein nanowires journal February 2020
Structure of Geobacter pili reveals secretory rather than nanowire behaviour journal September 2021
Electric field stimulates production of highly conductive microbial OmcZ nanowires journal August 2020
Low Energy Atomic Models Suggesting a Pilus Structure that could Account for Electrical Conductivity of Geobacter sulfurreducens Pili journal March 2016
On the electrical conductivity of microbial nanowires and biofilms journal January 2011
Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination journal January 2011
Conductivity of individual Geobacter pili journal January 2016
Rational design of electron/proton transfer mechanisms in the exoelectrogenic bacteria Geobacter sulfurreducens journal July 2021
Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens journal January 2003
Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms journal July 2006
Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1 journal October 2010
Long-range electron transport in Geobacter sulfurreducens biofilms is redox gradient-driven journal September 2012
Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components journal August 2014
Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography journal March 2018
Toward establishing minimum requirements for extracellular electron transfer in Geobacter sulfurreducens journal May 2017
Bacterial extracellular electron transfer in plant and animal ecosystems journal May 2023
Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens journal January 2013
Involvement of Geobacter sulfurreducens SfrAB in acetate metabolism rather than intracellular, respiration-linked Fe(III) citrate reduction journal October 2007
Electronic properties of conductive pili of the metal-reducing bacterium Geobacter sulfurreducens probed by scanning tunneling microscopy journal December 2011
Comparative proteomics of Geobacter sulfurreducens PCA T in response to acetate, formate and/or hydrogen as electron donor journal November 2020
A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by G eobacter sulfurreducens  PCA : A trans-outer membrane electron transfer complex journal September 2014
Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens journal October 2006
Specific localization of the c-type cytochrome OmcZ at the anode surface in current-producing biofilms of Geobacter sulfurreducens: c-type cytochrome accumulates at the electrode surface journal August 2010
Geobacter sulfurreducens inner membrane cytochrome CbcBA controls electron transfer and growth yield near the energetic limit of respiration journal September 2021
Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria journal December 2010
Direct Interspecies Electron Transfer between Geobacter metallireducens and Methanosarcina barkeri journal May 2014
Going Wireless: Fe(III) Oxide Reduction without Pili by Geobacter sulfurreducens Strain JS-1 journal May 2014
Biofilm and Nanowire Production Leads to Increased Current in Geobacter sulfurreducens Fuel Cells journal August 2006
Interspecies Electron Transfer via Hydrogen and Formate Rather than Direct Electrical Connections in Cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens journal August 2012
Proteolytic Maturation of the Outer Membrane c -Type Cytochrome OmcZ by a Subtilisin-Like Serine Protease Is Essential for Optimal Current Production by Geobacter sulfurreducens journal May 2021
Lack of Production of Electron-Shuttling Compounds or Solubilization of Fe(III) during Reduction of Insoluble Fe(III) Oxide by Geobacter metallireducens journal May 2000
Development of a Genetic System for Geobacter sulfurreducens journal July 2001
Electricity Production by Geobacter sulfurreducens Attached to Electrodes journal March 2003
Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens journal December 2005
Characterization of Metabolism in the Fe(III)-Reducing Organism Geobacter sulfurreducens by Constraint-Based Modeling journal February 2006
Electron Transport in the Dissimilatory Iron Reducer, GS-15 journal March 1991
Lack of Specificity in Geobacter Periplasmic Electron Transfer journal December 2022
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
Identification of Different Putative Outer Membrane Electron Conduits Necessary for Fe(III) Citrate, Fe(III) Oxide, Mn(IV) Oxide, or Electrode Reduction by Geobacter sulfurreducens journal July 2018
OmcB, a c-Type Polyheme Cytochrome, Involved in Fe(III) Reduction in Geobacter sulfurreducens journal April 2003
MacA, a Diheme c-Type Cytochrome Involved in Fe(III) Reduction by Geobacter sulfurreducens journal June 2004
Genetic Characterization of a Single Bifunctional Enzyme for Fumarate Reduction and Succinate Oxidation in Geobacter sulfurreducens and Engineering of Fumarate Reduction in Geobacter metallireducens journal January 2006
Structural Basis for Metallic-Like Conductivity in Microbial Nanowires journal March 2015
An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors journal November 2014
Electron Transfer Beyond the Outer Membrane: Putting Electrons to Rest journal September 2023
Dissimilatory Metal Reduction journal October 1993
Metabolic response of Geobacter sulfurreducens towards electron donor/acceptor variation journal January 2010
Biotechnological Aspects of Microbial Extracellular Electron Transfer journal January 2015
Computational and Experimental Analysis of Redundancy in the Central Metabolism of Geobacter sulfurreducens journal January 2008
Anode Biofilm Transcriptomics Reveals Outer Surface Components Essential for High Density Current Production in Geobacter sulfurreducens Fuel Cells journal May 2009
Analysis of Enhanced Current-Generating Mechanism of Geobacter sulfurreducens Strain via Model-Driven Metabolism Simulation journal September 2013
The Molecular Density of States in Bacterial Nanowires journal July 2008
Genomic analyses of bacterial porin-cytochrome gene clusters journal November 2014
Geobacter sulfurreducens Extracellular Multiheme Cytochrome PgcA Facilitates Respiration to Fe(III) Oxides But Not Electrodes journal December 2017
Putative Extracellular Electron Transfer in Methanogenic Archaea journal March 2021
Electron Flow From the Inner Membrane Towards the Cell Exterior in Geobacter sulfurreducens: Biochemical Characterization of Cytochrome CbcL journal May 2022
The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens journal October 2023
Genetic evidence that multiple cytochrome nanowires are necessary for Fe(III) oxide reduction in Geobacter sulfurreducens journal October 2023
Structure of Geobacter OmcZ filaments suggests extracellular cytochrome polymers evolved independently multiple times journal September 2022