skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria

Abstract

Extracellular electron transfer (EET) describes microbial bioelectrochemical processes in which electrons are transferred from the cytosol to the exterior of the cell1. Mineral-respiring bacteria use elaborate haem-based electron transfer mechanisms2,3,4 but the existence and mechanistic basis of other EETs remain largely unknown. Here we show that the food-borne pathogen Listeria monocytogenes uses a distinctive flavin-based EET mechanism to deliver electrons to iron or an electrode. By performing a forward genetic screen to identify L. monocytogenes mutants with diminished extracellular ferric iron reductase activity, we identified an eight-gene locus that is responsible for EET. This locus encodes a specialized NADH dehydrogenase that segregates EET from aerobic respiration by channelling electrons to a discrete membrane-localized quinone pool. Other proteins facilitate the assembly of an abundant extracellular flavoprotein that, in conjunction with free-molecule flavin shuttles, mediates electron transfer to extracellular acceptors. This system thus establishes a simple electron conduit that is compatible with the single-membrane structure of the Gram-positive cell. Activation of EET supports growth on non-fermentable carbon sources, and an EET mutant exhibited a competitive defect within the mouse gastrointestinal tract. Orthologues of the genes responsible for EET are present in hundreds of species across the Firmicutes phylum, including multiple pathogens andmore » commensal members of the intestinal microbiota, and correlate with EET activity in assayed strains. These findings suggest a greater prevalence of EET-based growth capabilities and establish a previously underappreciated relevance for electrogenic bacteria across diverse environments, including host-associated microbial communities and infectious disease.« less

Authors:
; ; ; ; ; ; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1574398
DOE Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
Nature (London)
Additional Journal Information:
Journal Volume: 562; Journal Issue: 7725; Journal ID: ISSN 0028-0836
Country of Publication:
United States
Language:
English

Citation Formats

Light, Samuel H., Su, Lin, Rivera-Lugo, Rafael, Cornejo, Jose A., Louie, Alexander, Iavarone, Anthony T., Ajo-Franklin, Caroline M., and Portnoy, Daniel A. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. United States: N. p., 2018. Web. doi:10.1038/s41586-018-0498-z.
Light, Samuel H., Su, Lin, Rivera-Lugo, Rafael, Cornejo, Jose A., Louie, Alexander, Iavarone, Anthony T., Ajo-Franklin, Caroline M., & Portnoy, Daniel A. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. United States. https://doi.org/10.1038/s41586-018-0498-z
Light, Samuel H., Su, Lin, Rivera-Lugo, Rafael, Cornejo, Jose A., Louie, Alexander, Iavarone, Anthony T., Ajo-Franklin, Caroline M., and Portnoy, Daniel A. Wed . "A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria". United States. https://doi.org/10.1038/s41586-018-0498-z.
@article{osti_1574398,
title = {A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria},
author = {Light, Samuel H. and Su, Lin and Rivera-Lugo, Rafael and Cornejo, Jose A. and Louie, Alexander and Iavarone, Anthony T. and Ajo-Franklin, Caroline M. and Portnoy, Daniel A.},
abstractNote = {Extracellular electron transfer (EET) describes microbial bioelectrochemical processes in which electrons are transferred from the cytosol to the exterior of the cell1. Mineral-respiring bacteria use elaborate haem-based electron transfer mechanisms2,3,4 but the existence and mechanistic basis of other EETs remain largely unknown. Here we show that the food-borne pathogen Listeria monocytogenes uses a distinctive flavin-based EET mechanism to deliver electrons to iron or an electrode. By performing a forward genetic screen to identify L. monocytogenes mutants with diminished extracellular ferric iron reductase activity, we identified an eight-gene locus that is responsible for EET. This locus encodes a specialized NADH dehydrogenase that segregates EET from aerobic respiration by channelling electrons to a discrete membrane-localized quinone pool. Other proteins facilitate the assembly of an abundant extracellular flavoprotein that, in conjunction with free-molecule flavin shuttles, mediates electron transfer to extracellular acceptors. This system thus establishes a simple electron conduit that is compatible with the single-membrane structure of the Gram-positive cell. Activation of EET supports growth on non-fermentable carbon sources, and an EET mutant exhibited a competitive defect within the mouse gastrointestinal tract. Orthologues of the genes responsible for EET are present in hundreds of species across the Firmicutes phylum, including multiple pathogens and commensal members of the intestinal microbiota, and correlate with EET activity in assayed strains. These findings suggest a greater prevalence of EET-based growth capabilities and establish a previously underappreciated relevance for electrogenic bacteria across diverse environments, including host-associated microbial communities and infectious disease.},
doi = {10.1038/s41586-018-0498-z},
url = {https://www.osti.gov/biblio/1574398}, journal = {Nature (London)},
issn = {0028-0836},
number = 7725,
volume = 562,
place = {United States},
year = {2018},
month = {9}
}

Works referenced in this record:

Fervidicella metallireducens gen. nov., sp. nov., a thermophilic, anaerobic bacterium from geothermal waters
journal, August 2009


Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors
journal, July 1997


Dissimilatory Reduction of Fe(III) by Thermophilic Bacteria and Archaea in Deep Subsurface Petroleum Reservoirs of Western Siberia
journal, August 1999


Thermovenabulum gondwanense sp. nov., a thermophilic anaerobic Fe(III)-reducing bacterium isolated from microbial mats thriving in a Great Artesian Basin bore runoff channel
journal, August 2009


Secretion of Flavins by Shewanella Species and Their Role in Extracellular Electron Transfer
journal, December 2007


Reduction of ferric iron by Listeria monocytogenes and other species of Listeria
journal, May 1993


Extracellular Electron Transfer Powers Enterococcus faecalis Biofilm Metabolism
journal, April 2018


Clustal W and Clustal X version 2.0
journal, September 2007


Orenia metallireducens sp. nov. Strain Z6, a Novel Metal-Reducing Member of the Phylum Firmicutes from the Deep Subsurface
journal, August 2016


Less label, more free: Approaches in label-free quantitative mass spectrometry
journal, January 2011


Identification of a Peptide-Pheromone that Enhances Listeria monocytogenes Escape from Host Cell Vacuoles
journal, March 2015


Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997


UPLC/MSE; a new approach for generating molecular fragment information for biomarker structure elucidation
journal, January 2006


InlA Promotes Dissemination of Listeria monocytogenes to the Mesenteric Lymph Nodes during Food Borne Infection of Mice
journal, November 2012


Flavins contained in yeast extract are exploited for anodic electron transfer by Lactococcus lactis
journal, June 2010


The PAMP c-di-AMP Is Essential for Listeria monocytogenes Growth in Rich but Not Minimal Media due to a Toxic Increase in (p)ppGpp
journal, June 2015


Shewanella secretes flavins that mediate extracellular electron transfer
journal, March 2008


Secretion of Bacterial Lipoproteins: Through the Cytoplasmic Membrane, the Periplasm and Beyond
journal, August 2014


UPLC/MSE; a new approach for generating molecular fragment information for biomarker structure elucidation
journal, January 2006


The Colorful World of Extracellular Electron Shuttles
journal, September 2017


Fervidicola ferrireducens gen. nov., sp. nov., a thermophilic anaerobic bacterium from geothermal waters of the Great Artesian Basin, Australia
journal, April 2009


Tools for Label-free Peptide Quantification
journal, December 2012


Listeria monocytogenes — from saprophyte to intracellular pathogen
journal, August 2009


Role of hemolysin for the intracellular growth of Listeria monocytogenes
journal, April 1988


Microbial Biofilm Voltammetry: Direct Electrochemical Characterization of Catalytic Electrode-Attached Biofilms
journal, October 2008


Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella
journal, November 2011


Aerobic Respiration Metabolism in Lactic Acid Bacteria and Uses in Biotechnology
journal, April 2012


Gut inflammation provides a respiratory electron acceptor for Salmonella
journal, September 2010


Listeria monocytogenes Is Resistant to Lysozyme through the Regulation, Not the Acquisition, of Cell Wall-Modifying Enzymes
journal, August 2014


Structure to function of an α-glucan metabolic pathway that promotes Listeria monocytogenes pathogenesis
journal, November 2016


MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016


ATP binding drives substrate capture in an ECF transporter by a release-and-catch mechanism
journal, June 2015


Riboflavin-shuttled extracellular electron transfer from Enterococcus faecalis to electrodes in microbial fuel cells
journal, November 2014


Effects of Traveling Wave Ion Mobility Separation on Data Independent Acquisition in Proteomics Studies
journal, May 2013


Alternative Pyrimidine Biosynthesis Protein ApbE Is a Flavin Transferase Catalyzing Covalent Attachment of FMN to a Threonine Residue in Bacterial Flavoproteins
journal, April 2013


Riboflavin (vitamin B-2) and health
journal, June 2003


Commensal microbes provide first line defense against Listeria monocytogenes infection
journal, June 2017


Extracellular Electron Transfer by the Gram-Positive Bacterium Enterococcus faecalis
journal, July 2018


Extracellular electron transfer mechanisms between microorganisms and minerals
journal, August 2016


Host-Derived Nitrate Boosts Growth of E. coli in the Inflamed Gut
journal, February 2013


Surface multiheme c-type cytochromes from Thermincola potens and implications for respiratory metal reduction by Gram-positive bacteria
journal, January 2012


Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis
journal, January 2013


Thermotalea metallivorans gen. nov., sp. nov., a thermophilic, anaerobic bacterium from the Great Artesian Basin of Australia aquifer
journal, April 2009


Novel Mode of Microbial Energy Metabolism: Organic Carbon Oxidation Coupled to Dissimilatory Reduction of Iron or Manganese
journal, January 1988


Organic Matter Mineralization with Reduction of Ferric Iron in Anaerobic Sediments
journal, January 1986


    Works referencing / citing this record:

    FeGenie: A Comprehensive Tool for the Identification of Iron Genes and Iron Gene Neighborhoods in Genome and Metagenome Assemblies
    journal, January 2020


    Electrical energy storage with engineered biological systems
    journal, May 2019


    Secreted Flavin Cofactors for Anaerobic Respiration of Fumarate and Urocanate by Shewanella oneidensis : Cost and Role
    journal, June 2019


    Effects of Flavin-Goethite Interaction on Goethite Reduction by Shewanella decolorationis S12
    journal, July 2019


    The Development of Biophotovoltaic Systems for Power Generation and Biological Analysis
    journal, September 2019


    Electroactive microorganisms in bioelectrochemical systems
    journal, March 2019


    Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option
    journal, January 2020


    Simple animal models for microbiome research
    journal, August 2019


    Impact of iron reduction on the metabolism of Clostridium acetobutylicum
    journal, May 2019


    Enhancing bioelectricity generation in microbial fuel cells and biophotovoltaics using nanomaterials
    journal, June 2019


    Charge Transport through Self‐Assembled Monolayers of Monoterpenoids
    journal, May 2019


    From Microbial Fuel Cells to Biobatteries: Moving toward On‐Demand Micropower Generation for Small‐Scale Single‐Use Applications
    journal, March 2019


    Mutational analysis of the flavinylation and binding motifs in two protein targets of the flavin transferase ApbE
    journal, November 2019


    Efficient biohydrogen and bioelectricity production from xylose by microbial fuel cell with newly isolated yeast of Cystobasidium slooffiae
    journal, September 2019


    Microfluidic dielectrophoresis illuminates the relationship between microbial cell envelope polarizability and electrochemical activity
    journal, January 2019


    Molecular underpinnings for microbial extracellular electron transfer during biogeochemical cycling of earth elements
    journal, March 2019


    Charge Transport through Self‐Assembled Monolayers of Monoterpenoids
    journal, June 2019


    Shigella-mediated oxygen depletion is essential for intestinal mucosa colonization
    journal, August 2019


    Biofilms 2018: a Diversity of Microbes and Mechanisms
    journal, February 2019


    Characterizing the Anoxic Phenotype of Pseudomonas putida Using a Bioelectrochemical System
    journal, March 2019


    Interdependency of Respiratory Metabolism and Phenazine-Associated Physiology in Pseudomonas aeruginosa PA14
    journal, November 2019


    Stimulation of Smithella ‐dominating propionate oxidation in a sediment enrichment by magnetite and carbon nanotubes
    journal, March 2019