scholarly journals Regulation of Gene Expression in Shewanella oneidensis MR-1 during Electron Acceptor Limitation and Bacterial Nanowire Formation

2016 ◽  
Vol 82 (17) ◽  
pp. 5428-5443 ◽  
Author(s):  
Sarah E. Barchinger ◽  
Sahand Pirbadian ◽  
Christine Sambles ◽  
Carol S. Baker ◽  
Kar Man Leung ◽  
...  
Keyword(s):  
Gene Expression ◽  
Electron Transfer ◽  
Outer Membrane ◽  
Electron Acceptor ◽  
Shewanella Oneidensis ◽  
Oxygen Limitation ◽  
Extracellular Electron Transfer ◽  
Transport Pathways ◽  
Content Type ◽  
Genes Encoding

ABSTRACTIn limiting oxygen as an electron acceptor, the dissimilatory metal-reducing bacteriumShewanella oneidensisMR-1 rapidly forms nanowires, extensions of its outer membrane containing the cytochromes MtrC and OmcA needed for extracellular electron transfer. RNA sequencing (RNA-Seq) analysis was employed to determine differential gene expression over time from triplicate chemostat cultures that were limited for oxygen. We identified 465 genes with decreased expression and 677 genes with increased expression. The coordinated increased expression of heme biosynthesis, cytochrome maturation, and transport pathways indicates thatS. oneidensisMR-1 increases cytochrome production, including the transcription of genes encoding MtrA, MtrC, and OmcA, and transports these decaheme cytochromes across the cytoplasmic membrane during electron acceptor limitation and nanowire formation. In contrast, the expression of themtrAandmtrChomologsmtrFandmtrDeither remains unaffected or decreases under these conditions. TheompWgene, encoding a small outer membrane porin, has 40-fold higher expression during oxygen limitation, and it is proposed that OmpW plays a role in cation transport to maintain electrical neutrality during electron transfer. The genes encoding the anaerobic respiration regulator cyclic AMP receptor protein (CRP) and the extracytoplasmic function sigma factor RpoE are among the transcription factor genes with increased expression. RpoE might function by signaling the initial response to oxygen limitation. Our results show that RpoE activates transcription from promoters upstream ofmtrCandomcA. The transcriptome and mutant analyses ofS. oneidensisMR-1 nanowire production are consistent with independent regulatory mechanisms for extending the outer membrane into tubular structures and for ensuring the electron transfer function of the nanowires.IMPORTANCEShewanella oneidensisMR-1 has the capacity to transfer electrons to its external surface using extensions of the outer membrane called bacterial nanowires. These bacterial nanowires link the cell's respiratory chain to external surfaces, including oxidized metals important in bioremediation, and explain whyS. oneidensiscan be utilized as a component of microbial fuel cells, a form of renewable energy. In this work, we use differential gene expression analysis to focus on which genes function to produce the nanowires and promote extracellular electron transfer during oxygen limitation. Among the genes that are expressed at high levels are those encoding cytochrome proteins necessary for electron transfer.Shewanellacoordinates the increased expression of regulators, metabolic pathways, and transport pathways to ensure that cytochromes efficiently transfer electrons along the nanowires.

scholarly journals Divergent Nrf Family Proteins and MtrCAB Homologs Facilitate Extracellular Electron Transfer inAeromonas hydrophila

2018 ◽  
Vol 84 (23) ◽  
Author(s):  
Bridget E. Conley ◽  
Peter J. Intile ◽  
Daniel R. Bond ◽  
Jeffrey A. Gralnick
Keyword(s):  
Electron Transfer ◽  
Outer Membrane ◽  
Aeromonas Hydrophila ◽  
Shewanella Oneidensis ◽  
Geobacter Sulfurreducens ◽  
Model Systems ◽  
Extracellular Electron Transfer ◽  
Metal Reduction ◽  
Inner Membrane ◽  
Content Type

ABSTRACTExtracellular electron transfer (EET) is a strategy for respiration in which electrons generated from metabolism are moved outside the cell to a terminal electron acceptor, such as iron or manganese oxide. EET has primarily been studied in two model systems,Shewanella oneidensisandGeobacter sulfurreducens. Metal reduction has also been reported in numerous microorganisms, includingAeromonasspp., which are ubiquitousGammaproteobacteriafound in aquatic ecosystems, with some species capable of pathogenesis in humans and fish. Genomic comparisons ofAeromonasspp. revealed a potential outer membrane conduit homologous toS. oneidensisMtrCAB. While the ability to respire metals and mineral oxides is not widespread in the genusAeromonas, 90% of the sequencedAeromonas hydrophilaisolates contain MtrCAB homologs.A. hydrophilaATCC 7966 mutants lackingmtrAare unable to reduce metals. Expression ofA. hydrophila mtrCABin anS. oneidensismutant lacking homologous components restored metal reduction. Although the outer membrane conduits for metal reduction were similar, homologs of theS. oneidensisinner membrane and periplasmic EET components CymA, FccA, and CctA were not found inA. hydrophila. We characterized a cluster of genes predicted to encode components related to a formate-dependent nitrite reductase (NrfBCD), here named NetBCD (forNrf-likeelectrontransfer), and a predicted diheme periplasmic cytochrome, PdsA (periplasmicdihemeshuttle). We present genetic evidence that proteins encoded by this cluster facilitate electron transfer from the cytoplasmic membrane across the periplasm to the MtrCAB conduit and function independently from an authentic NrfABCD system.A. hydrophilamutants lackingpdsAandnetBCDwere unable to reduce metals, while heterologous expression of these genes could restore metal reduction in anS. oneidensismutant background. EET may therefore allowA. hydrophilaand other species ofAeromonasto persist and thrive in iron- or manganese-rich oxygen-limited environments.IMPORTANCEMetal-reducing microorganisms are used for electricity production, bioremediation of toxic compounds, wastewater treatment, and production of valuable compounds. Despite numerous microorganisms being reported to reduce metals, the molecular mechanism has primarily been studied in two model systems,Shewanella oneidensisandGeobacter sulfurreducens. We have characterized the mechanism of extracellular electron transfer inAeromonas hydrophila, which uses the well-studiedShewanellasystem, MtrCAB, to move electrons across the outer membrane; however, mostAeromonasspp. appear to use a novel mechanism to transfer electrons from the inner membrane through the periplasm and to the outer membrane. The conserved use of MtrCAB inShewanellaspp. andAeromonasspp. for metal reduction and conserved genomic architecture of metal reduction genes inAeromonasspp. may serve as genomic markers for identifying metal-reducing microorganisms from genomic or transcriptomic sequencing. Understanding the variety of pathways used to reduce metals can allow for optimization and more efficient design of microorganisms used for practical applications.

scholarly journals A Hybrid Extracellular Electron Transfer Pathway Enhances the Survival of Vibrio natriegens

2020 ◽  
Vol 86 (19) ◽  
Author(s):  
Bridget E. Conley ◽  
Matthew T. Weinstock ◽  
Daniel R. Bond ◽  
Jeffrey A. Gralnick
Keyword(s):  
Electron Transfer ◽  
Shewanella Oneidensis ◽  
Anaerobic Respiration ◽  
Basic Research ◽  
Extracellular Electron Transfer ◽  
Content Type ◽  
Electron Transfer Pathway ◽  
Sedimentary Environments ◽  
Genetic Potential ◽  
Iron And Manganese

ABSTRACT Vibrio natriegens is the fastest-growing microorganism discovered to date, making it a useful model for biotechnology and basic research. While it is recognized for its rapid aerobic metabolism, less is known about anaerobic adaptations in V. natriegens or how the organism survives when oxygen is limited. Here, we describe and characterize extracellular electron transfer (EET) in V. natriegens, a metabolism that requires movement of electrons across protective cellular barriers to reach the extracellular space. V. natriegens performs extracellular electron transfer under fermentative conditions with gluconate, glucosamine, and pyruvate. We characterized a pathway in V. natriegens that requires CymA, PdsA, and MtrCAB for Fe(III) citrate and Fe(III) oxide reduction, which represents a hybrid of strategies previously discovered in Shewanella and Aeromonas. Expression of these V. natriegens genes functionally complemented Shewanella oneidensis mutants. Phylogenetic analysis of the inner membrane quinol dehydrogenases CymA and NapC in gammaproteobacteria suggests that CymA from Shewanella diverged from Vibrionaceae CymA and NapC. Analysis of sequenced Vibrionaceae revealed that the genetic potential to perform EET is conserved in some members of the Harveyi and Vulnificus clades but is more variable in other clades. We provide evidence that EET enhances anaerobic survival of V. natriegens, which may be the primary physiological function for EET in Vibrionaceae. IMPORTANCE Bacteria from the genus Vibrio occupy a variety of marine and brackish niches with fluctuating nutrient and energy sources. When oxygen is limited, fermentation or alternative respiration pathways must be used to conserve energy. In sedimentary environments, insoluble oxide minerals (primarily iron and manganese) are able to serve as electron acceptors for anaerobic respiration by microorganisms capable of extracellular electron transfer, a metabolism that enables the use of these insoluble substrates. Here, we identify the mechanism for extracellular electron transfer in Vibrio natriegens, which uses a combination of strategies previously identified in Shewanella and Aeromonas. We show that extracellular electron transfer enhanced survival of V. natriegens under fermentative conditions, which may be a generalized strategy among Vibrio spp. predicted to have this metabolism.

scholarly journals Identification of Different Putative Outer Membrane Electron Conduits Necessary for Fe(III) Citrate, Fe(III) Oxide, Mn(IV) Oxide, or Electrode Reduction byGeobacter sulfurreducens

2018 ◽  
Vol 200 (19) ◽  
Author(s):  
Fernanda Jiménez Otero ◽  
Chi Ho Chan ◽  
Daniel R. Bond
Keyword(s):  
Electron Transfer ◽  
Outer Membrane ◽  
Electron Acceptor ◽  
Gene Clusters ◽  
Geobacter Sulfurreducens ◽  
Transcriptional Analysis ◽  
Metal Reduction ◽  
Wild Type ◽  
Redox Proteins ◽  
Content Type

ABSTRACTAt least five gene clusters in theGeobacter sulfurreducensgenome encode putative “electron conduits” implicated in electron transfer across the outer membrane, each containing a periplasmic multihemec-type cytochrome, integral outer membrane anchor, and outer membrane redox lipoprotein(s). Markerless single-gene-cluster deletions and all possible multiple-deletion combinations were constructed and grown with soluble Fe(III) citrate, Fe(III) and Mn(IV) oxides, and graphite electrodes poised at +0.24 V and −0.1 V versus the standard hydrogen electrode (SHE). Different gene clusters were necessary for reduction of each electron acceptor. During metal oxide reduction, deletion of the previously describedomcBCcluster caused defects, but deletion of additional components in an ΔomcBCbackground, such asextEFG, were needed to produce defects greater than 50% compared to findings with the wild type. Deletion of all five gene clusters abolished all metal reduction. During electrode reduction, only the ΔextABCDmutant had a severe growth defect at both redox potentials, while this mutation did not affect Fe(III) oxide, Mn(IV) oxide, or Fe(III) citrate reduction. Some mutants containing only one cluster were able to reduce particular terminal electron acceptors better than the wild type, suggesting routes for improvement by targeting specific electron transfer pathways. Transcriptomic comparisons between fumarate and electrode-based growth conditions showed all of theseextclusters to be constitutive, and transcriptional analysis of the triple-deletion strain containing onlyextABCDdetected no significant changes in expression of genes encoding known redox proteins or pilus components. These genetic experiments reveal new outer membrane conduit complexes necessary for growth ofG. sulfurreducens, depending on the available extracellular electron acceptor.IMPORTANCEGram-negative metal-reducing bacteria utilize electron conduits, chains of redox proteins spanning the outer membrane, to transfer electrons to the extracellular surface. Only one pathway for electron transfer across the outer membrane ofGeobacter sulfurreducenshas been linked to Fe(III) reduction. However,G. sulfurreducensis able to respire a wide array of extracellular substrates. Here we present the first combinatorial genetic analysis of five different electron conduits via creation of new markerless deletion strains and complementation vectors. Multiple conduit gene clusters appear to have overlapping roles, including two that have never been linked to metal reduction. Another recently described cluster (ExtABCD) was the only electron conduit essential during electrode reduction, a substrate of special importance to biotechnological applications of this organism.

scholarly journals Geothrix fermentans Secretes Two Different Redox-Active Compounds To Utilize Electron Acceptors across a Wide Range of Redox Potentials

2012 ◽  
Vol 78 (19) ◽  
pp. 6987-6995 ◽  
Author(s):  
Misha G. Mehta-Kolte ◽  
Daniel R. Bond
Keyword(s):  
Electron Transfer ◽  
Redox Potential ◽  
Electron Acceptor ◽  
Extracellular Electron Transfer ◽  
Redox Potentials ◽  
Active Compounds ◽  
Content Type ◽  
Electron Shuttles ◽  
Redox Active ◽  
Geothrix Fermentans

ABSTRACTThe current understanding of dissimilatory metal reduction is based primarily on isolates from the proteobacterial generaGeobacterandShewanella. However, environments undergoing active Fe(III) reduction often harbor less-well-studied phyla that are equally abundant. In this work, electrochemical techniques were used to analyze respiratory electron transfer by the only known Fe(III)-reducing representative of theAcidobacteria,Geothrix fermentans. In contrast to previously characterized metal-reducing bacteria, which typically reach maximal rates of respiration at electron acceptor potentials of 0 V versus standard hydrogen electrode (SHE),G. fermentansrequired potentials as high as 0.55 V to respire at its maximum rate. In addition,G. fermentanssecreted two different soluble redox-active electron shuttles with separate redox potentials (−0.2 V and 0.3 V). The compound with the lower midpoint potential, responsible for 20 to 30% of electron transfer activity, was riboflavin. The behavior of the higher-potential compound was consistent with hydrophilic UV-fluorescent molecules previously found inG. fermentanssupernatants. Both electron shuttles were also produced when cultures were grown with Fe(III), but not when fumarate was the electron acceptor. This study reveals thatGeothrixis able to take advantage of higher-redox-potential environments, demonstrates that secretion of flavin-based shuttles is not confined toShewanella, and points to the existence of high-potential-redox-active compounds involved in extracellular electron transfer. Based on differences between the respiratory strategies ofGeothrixandGeobacter, these two groups of bacteria could exist in distinctive environmental niches defined by redox potential.

scholarly journals Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis

mBio ◽  
2013 ◽  
Vol 4 (1) ◽  
Author(s):  
Nicholas J. Kotloski ◽  
Jeffrey A. Gralnick
Keyword(s):  
Electron Transfer ◽  
Direct Electron Transfer ◽  
Shewanella Oneidensis ◽  
Phenotypic Characterization ◽  
Extracellular Electron Transfer ◽  
Wild Type ◽  
Content Type ◽  
Electron Shuttling ◽  
Electron Shuttles ◽  
Set Up

ABSTRACT Shewanella oneidensis strain MR-1 is widely studied for its ability to respire a diverse array of soluble and insoluble electron acceptors. The ability to breathe insoluble substrates is defined as extracellular electron transfer and can occur via direct contact or by electron shuttling in S. oneidensis. To determine the contribution of flavin electron shuttles in extracellular electron transfer, a transposon mutagenesis screen was performed with S. oneidensis to identify mutants unable to secrete flavins. A multidrug and toxin efflux transporter encoded by SO_0702 was identified and renamed bfe (bacterial flavin adenine dinucleotide [FAD] exporter) based on phenotypic characterization. Deletion of bfe resulted in a severe decrease in extracellular flavins, while overexpression of bfe increased the concentration of extracellular flavins. Strains lacking bfe had no defect in reduction of soluble Fe(III), but these strains were deficient in the rate of insoluble Fe(III) oxide reduction, which was alleviated by the addition of exogenous flavins. To test a different insoluble electron acceptor, graphite electrode bioreactors were set up to measure current produced by wild-type S. oneidensis and the Δbfe mutant. With the same concentration of supplemented flavins, the two strains produced similar amounts of current. However, when exogenous flavins were not supplemented to bioreactors, bfe mutant strains produced significantly less current than the wild type. We have demonstrated that flavin electron shuttling accounts for ~75% of extracellular electron transfer to insoluble substrates by S. oneidensis and have identified the first FAD transporter in bacteria. IMPORTANCE Extracellular electron transfer by microbes is critical for the geochemical cycling of metals, bioremediation, and biocatalysis using electrodes. A controversy in the field was addressed by demonstrating that flavin electron shuttling, not direct electron transfer or nanowires, is the primary mechanism of extracellular electron transfer employed by the bacterium Shewanella oneidensis. We have identified a flavin adenine dinucleotide transporter conserved in all sequenced Shewanella species that facilitates export of flavin electron shuttles in S. oneidensis. Analysis of a strain that is unable to secrete flavins demonstrated that electron shuttling accounts for ~75% of the insoluble extracellular electron transfer capacity in S. oneidensis.

scholarly journals Outer Membrane c-Type Cytochromes OmcA and MtrC Play Distinct Roles in Enhancing the Attachment of Shewanella oneidensis MR-1 Cells to Goethite

2020 ◽  
Vol 86 (23) ◽  
Author(s):  
Xinxin Jing ◽  
Yichao Wu ◽  
Liang Shi ◽  
Caroline L. Peacock ◽  
Noha Mohamed Ashry ◽  
...  
Keyword(s):  
Cell Surface ◽  
Outer Membrane ◽  
Interfacial Reaction ◽  
Contact Area ◽  
Protein Structures ◽  
Shewanella Oneidensis ◽  
Molecular Structures ◽  
Attractive Force ◽  
Extracellular Electron Transfer ◽  
Content Type

ABSTRACT The outer membrane c-type cytochromes (c-Cyts) OmcA and MtrC in Shewanella are key terminal reductases that bind and transfer electrons directly to iron (hydr)oxides. Although the amounts of OmcA and MtrC at the cell surface and their molecular structures are largely comparable, MtrC is known to play a more important role in dissimilatory iron reduction. To explore the roles of these outer membrane c-Cyts in the interaction of Shewanella oneidensis MR-1 with iron oxides, the processes of attachment of S. oneidensis MR-1 wild type and c-type cytochrome-deficient mutants (the ΔomcA, ΔmtrC, and ΔomcA ΔmtrC mutants) to goethite are compared via quartz crystal microbalance with dissipation monitoring (QCM-D). Strains with OmcA exhibit a rapid initial attachment. The quantitative model for QCM-D responses reveals that MtrC enhances the contact area and contact elasticity of cells with goethite by more than one and two times, respectively. In situ attenuated total reflectance Fourier transform infrared two-dimensional correlation spectroscopic (ATR-FTIR 2D-CoS) analysis shows that MtrC promotes the initial interfacial reaction via an inner-sphere coordination. Atomic force microscopy (AFM) analysis demonstrates that OmcA enhances the attractive force between cells and goethite by about 60%. As a result, OmcA contributes to a higher attractive force with goethite and induces a rapid short-term attachment, while MtrC is more important in the longer-term interaction through an enhanced contact area, which promotes interfacial reactions. These results reveal that c-Cyts OmcA and MtrC adopt different mechanisms for enhancing the attachment of S. oneidensis MR-1 cells to goethite. It improves our understanding of the function of outer membrane c-Cyts and the influence of cell surface macromolecules in cell-mineral interactions. IMPORTANCE Shewanella species are one group of versatile and widespread dissimilatory iron-reducing bacteria, which are capable of respiring insoluble iron minerals via six multiheme c-type cytochromes. Outer membrane c-type cytochromes (c-Cyts) OmcA and MtrC are the terminal reductases in this pathway and have comparable protein structures. In this study, we elucidate the different roles of OmcA and MtrC in the interaction of S. oneidensis MR-1 with goethite at the whole-cell level. OmcA confers enhanced affinity toward goethite and results in rapid attachment. Meanwhile, MtrC significantly increases the contact area of bacterial cells with goethite and promotes the interfacial reaction, which may explain its central role in extracellular electron transfer. This study provides novel insights into the role of bacterial surface macromolecules in the interfacial interaction of bacteria with minerals, which is critical to the development of a comprehensive understanding of cell-mineral interactions.

scholarly journals Genetic Control of Radical Crosslinking in a Semi-Synthetic Hydrogel

2019 ◽  
Author(s):  
Austin J. Graham ◽  
Christopher M. Dundas ◽  
Alexander Hillsley ◽  
Dain S. Kasprak ◽  
Adrianne M. Rosales ◽  
...  
Keyword(s):  
Gene Expression ◽  
Electron Transfer ◽  
Genetic Control ◽  
Storage Modulus ◽  
Material Properties ◽  
Shewanella Oneidensis ◽  
General Mechanism ◽  
Extracellular Electron Transfer ◽  
Metal Catalyst ◽  
Next Generation

AbstractEnhancing materials with the qualities of living systems, including sensing, computation, and adaptation, is an important challenge in designing next-generation technologies. Living materials seek to address this challenge by incorporating live cells as actuating components that control material function. For abiotic materials, this requires new methods that couple genetic and metabolic processes to material properties. Toward this goal, we demonstrate that extracellular electron transfer (EET) from Shewanella oneidensis can be leveraged to control radical crosslinking of a methacrylate-functionalized hyaluronic acid hydrogel. Crosslinking rates and hydrogel mechanics, specifically storage modulus, were dependent on a variety of chemical and biological factors, including S. oneidensis genotype. Bacteria remained viable and metabolically active in the crosslinked network for a least one week, while cell tracking revealed that EET genes also encode control over hydrogel microstructure. Moreover, construction of an inducible gene circuit allowed transcriptional control of storage modulus and crosslinking rate via the tailored expression of a key electron transfer protein, MtrC. Finally, we quantitatively modeled dependence of hydrogel stiffness on steady-state gene expression, and generalized this result by demonstrating the strong relationship between relative gene expression and material properties. This general mechanism for radical crosslinking provides a foundation for programming the form and function of synthetic materials through genetic control over extracellular electron transfer.Significance StatementNext-generation materials will require coupling the advantages of engineered and natural systems to solve complex challenges in energy, health, and the environment. Living cells, such as bacteria, naturally possess many of the qualities essential to addressing these challenges, including sensing, computation, and actuation, using their genetic and metabolic machinery. In addition, bacteria are attractive for incorporation into materials due to their durability, ease-of-use, and programmability. Here, we develop a platform for controlling hydrogel properties (e.g., stiffness, crosslinking rate) using extracellular electron transfer from the bacterium Shewanella oneidensis. In our system, metabolic electron flux from S. oneidensis to a metal catalyst generates radical species that crosslink an acrylate-based macromer to form the gel. This synthetic reaction is under direct control of bacterial genetics and metabolism, which we demonstrate through inducible circuits and quantitative modeling of gene expression and resultant hydrogel properties. Developing methods that capitalize on the programmability of biological systems to control synthetic material properties will enable hybrid material designs with unprecedented functions.

scholarly journals A Membrane-Bound Cytochrome Enables Methanosarcina acetivorans To Conserve Energy from Extracellular Electron Transfer

mBio ◽  
2019 ◽  
Vol 10 (4) ◽  
Author(s):  
Dawn E. Holmes ◽  
Toshiyuki Ueki ◽  
Hai-Yan Tang ◽  
Jinjie Zhou ◽  
Jessica A. Smith ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Electron Acceptor ◽  
Methane Production ◽  
Genetic Manipulation ◽  
Methanol Conversion ◽  
Extracellular Electron Transfer ◽  
Methanosarcina Acetivorans ◽  
Coenzyme M ◽  
Content Type ◽  
Expression Of Genes

ABSTRACT Extracellular electron exchange in Methanosarcina species and closely related Archaea plays an important role in the global carbon cycle and enhances the speed and stability of anaerobic digestion by facilitating efficient syntrophic interactions. Here, we grew Methanosarcina acetivorans with methanol provided as the electron donor and the humic analogue, anthraquione-2,6-disulfonate (AQDS), provided as the electron acceptor when methane production was inhibited with bromoethanesulfonate. AQDS was reduced with simultaneous methane production in the absence of bromoethanesulfonate. Transcriptomics revealed that expression of the gene for the transmembrane, multiheme, c-type cytochrome MmcA was higher in AQDS-respiring cells than in cells performing methylotrophic methanogenesis. A strain in which the gene for MmcA was deleted failed to grow via AQDS reduction but grew with the conversion of methanol or acetate to methane, suggesting that MmcA has a specialized role as a conduit for extracellular electron transfer. Enhanced expression of genes for methanol conversion to methyl-coenzyme M and the Rnf complex suggested that methanol is oxidized to carbon dioxide in AQDS-respiring cells through a pathway that is similar to methyl-coenzyme M oxidation in methanogenic cells. However, during AQDS respiration the Rnf complex and reduced methanophenazine probably transfer electrons to MmcA, which functions as the terminal reductase for AQDS reduction. Extracellular electron transfer may enable the survival of methanogens in dynamic environments in which oxidized humic substances and Fe(III) oxides are intermittently available. The availability of tools for genetic manipulation of M. acetivorans makes it an excellent model microbe for evaluating c-type cytochrome-dependent extracellular electron transfer in Archaea. IMPORTANCE The discovery of a methanogen that can conserve energy to support growth solely from the oxidation of organic carbon coupled to the reduction of an extracellular electron acceptor expands the possible environments in which methanogens might thrive. The potential importance of c-type cytochromes for extracellular electron transfer to syntrophic bacterial partners and/or Fe(III) minerals in some Archaea was previously proposed, but these studies with Methanosarcina acetivorans provide the first genetic evidence for cytochrome-based extracellular electron transfer in Archaea. The results suggest parallels with Gram-negative bacteria, such as Shewanella and Geobacter species, in which multiheme outer-surface c-type cytochromes are an essential component for electrical communication with the extracellular environment. M. acetivorans offers an unprecedented opportunity to study mechanisms for energy conservation from the anaerobic oxidation of one-carbon organic compounds coupled to extracellular electron transfer in Archaea with implications not only for methanogens but possibly also for Archaea that anaerobically oxidize methane.

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