scholarly journals SyntrophusConductive Pili Demonstrate that Common Hydrogen-Donating Syntrophs can have a Direct Electron Transfer Option

2018 ◽  
Author(s):  
David J.F. Walker ◽  
Kelly P. Nevin ◽  
Dawn E. Holmes ◽  
Amelia-Elena Rotaru ◽  
Joy E. Ward ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Microbial Communities ◽  
Direct Electron Transfer ◽  
Electron Exchange ◽  
Practical Significance ◽  
Electrically Conductive ◽  
Interspecies Electron Transfer ◽  
Primary Mechanism ◽  
Electron Carriers ◽  
Syntrophus Aciditrophicus

AbstractSyntrophic interspecies electron exchange is essential for the stable functioning of diverse anaerobic microbial communities. Hydrogen/formate interspecies electron transfer (HFIT), in which H2and/or formate function as diffusible electron carriers, has been considered to be the primary mechanism for electron sharing because most common syntrophs were thought to lack biochemical components, such as electrically conductive pili (e-pili), necessary for direct interspecies electron transfer (DIET). Here we report thatSyntrophus aciditrophicus, one of the most intensively studied microbial models for HFIT, produces e-pili and can grow via DIET. Pilin genes likely to yield e-pili were found in other genera of hydrogen/formate-producing syntrophs. The finding that DIET is a likely option for diverse syntrophs that are abundant in many anaerobic environments necessitates a reexamination of the paradigm that HFIT is the predominant mechanism for syntrophic electron exchange within anaerobic microbial communities of biogeochemical and practical significance.

Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange

2013 ◽  
Vol 5 (6) ◽  
pp. 904-910 ◽  
Author(s):  
Pravin Malla Shrestha ◽  
Amelia-Elena Rotaru ◽  
Muktak Aklujkar ◽  
Fanghua Liu ◽  
Minita Shrestha ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Energy Exchange ◽  
Direct Interspecies Electron Transfer ◽  
Interspecies Electron Transfer ◽  
Primary Mechanism

scholarly journals Modeling of interspecies electron transfer in anaerobic microbial communities

2021 ◽  
Vol 67 ◽  
pp. 49-57
Author(s):  
Elie Desmond-Le Quéméner ◽  
Roman Moscoviz ◽  
Nicolas Bernet ◽  
Andrew Marcus
Keyword(s):  
Electron Transfer ◽  
Microbial Communities ◽  
Interspecies Electron Transfer

scholarly journals Mechanisms for Electron Uptake by Methanosarcina acetivorans During Direct Interspecies Electron Transfer

2021 ◽  
Author(s):  
Dawn Holmes ◽  
Jinjie Zhou ◽  
Toshiyuki Ueki ◽  
Trevor Woodard ◽  
Derek Lovley
Keyword(s):  
Carbon Dioxide ◽  
Electron Transfer ◽  
Outer Surface ◽  
Expression Patterns ◽  
Amino Acid Content ◽  
Carbon Dioxide Reduction ◽  
Methanosarcina Acetivorans ◽  
Electrically Conductive ◽  
Direct Interspecies Electron Transfer ◽  
Interspecies Electron Transfer

Direct interspecies electron transfer (DIET) between bacteria and methanogenic archaea appears to be an important syntrophy in both natural and engineered methanogenic environments. However, the electrical connections on the outer surface of methanogens and the subsequent processing of electrons for carbon dioxide reduction to methane are poorly understood. Here we report that the genetically tractable methanogen Methanosarcina acetivorans can grow via DIET in co-culture with Geobacter metallireducens serving as the electron-donating partner. Comparison of gene expression patterns in M. acetivorans grown in co-culture versus pure culture growth on acetate revealed that transcripts for the outer-surface, multi-heme, c-type cytochrome MmcA were higher during DIET-based growth. Deletion of mmcA inhibited DIET. The high aromatic amino acid content of M. acetivorans archaellins suggests that they might assemble into electrically conductive archaella. A mutant that could not express archaella was deficient in DIET. However, this mutant grew in DIET-based co-culture as well as the archaella-expressing parental strain in the presence of granular activated carbon, which was previously shown to serve as a substitute for electrically conductive pili as a conduit for long-range interspecies electron transfer in other DIET-based co-cultures. Transcriptomic data suggesting that the membrane-bound Rnf, Fpo, and HdrED complexes also play a role in DIET were incorporated into a charge-balanced model illustrating how electrons entering the cell through MmcA can yield energy to support growth from carbon dioxide reduction. The results are the first genetics-based functional demonstration of likely outer-surface electrical contacts for DIET in a methanogen.

scholarly journals Potential for Direct Interspecies Electron Transfer in Methanogenic Wastewater Digester Aggregates

mBio ◽  
2011 ◽  
Vol 2 (4) ◽  
Author(s):  
Masahiko Morita ◽  
Nikhil S. Malvankar ◽  
Ashley E. Franks ◽  
Zarath M. Summers ◽  
Ludovic Giloteaux ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Organic Matter ◽  
Geobacter Sulfurreducens ◽  
Anaerobic Sludge ◽  
Rrna Gene ◽  
Electrically Conductive ◽  
Content Type ◽  
Direct Interspecies Electron Transfer ◽  
Interspecies Electron Transfer ◽  
Anaerobic Soils

ABSTRACTMechanisms for electron transfer within microbial aggregates derived from an upflow anaerobic sludge blanket reactor converting brewery waste to methane were investigated in order to better understand the function of methanogenic consortia. The aggregates were electrically conductive, with conductivities 3-fold higher than the conductivities previously reported for dual-species aggregates ofGeobacterspecies in which the two species appeared to exchange electrons via interspecies electron transfer. The temperature dependence response of the aggregate conductance was characteristic of the organic metallic-like conductance previously described for the conductive pili ofGeobacter sulfurreducensand was inconsistent with electron conduction through minerals. Studies in which aggregates were incubated with high concentrations of potential electron donors demonstrated that the aggregates had no significant capacity for conversion of hydrogen to methane. The aggregates converted formate to methane but at rates too low to account for the rates at which that the aggregates syntrophically metabolized ethanol, an important component of the reactor influent.Geobacterspecies comprised 25% of 16S rRNA gene sequences recovered from the aggregates, suggesting thatGeobacterspecies may have contributed to some but probably not all of the aggregate conductivity. Microorganisms most closely related to the acetate-utilizingMethanosaeta conciliiaccounted for more than 90% of the sequences that could be assigned to methane producers, consistent with the poor capacity for hydrogen and formate utilization. These results demonstrate for the first time that methanogenic wastewater aggregates can be electrically conductive and suggest that direct interspecies electron transfer could be an important mechanism for electron exchange in some methanogenic systems.IMPORTANCEThe conversion of waste organic matter to methane is an important bioenergy strategy, and a similar microbial metabolism of complex organic matter in anaerobic soils and sediments plays an important role in the global carbon cycle. Studies with laboratory cultures have demonstrated that hydrogen or formate can serve as an electron shuttle between the microorganisms degrading organic compounds and methanogens. However, the importance of hydrogen and formate as intermediates in the conversion of organic matter to methane in natural communities is less clear. The possibility that microorganisms within some natural methanogenic aggregates may directly exchange electrons, rather than producing hydrogen or formate as an intermediary electron carrier, is a significant paradigm shift with implications for the modeling and design of anaerobic wastewater reactors and for understanding how methanogenic communities will respond to environmental perturbations.

Syntrophy and Interspecies Electron Transfer in Methanogenic Microbial Communities

Microbiology ◽  
2020 ◽  
Vol 89 (2) ◽  
pp. 129-147 ◽  
Author(s):  
A. N. Nozhevnikova ◽  
Yu. I. Russkova ◽  
Yu. V. Litti ◽  
S. N. Parshina ◽  
E. A. Zhuravleva ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Microbial Communities ◽  
Interspecies Electron Transfer

scholarly journals Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea

mBio ◽  
2017 ◽  
Vol 8 (4) ◽  
Author(s):  
Connor T. Skennerton ◽  
Karuna Chourey ◽  
Ramsunder Iyer ◽  
Robert L. Hettich ◽  
Gene W. Tyson ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Direct Electron Transfer ◽  
Sulfate Reducing Bacteria ◽  
Recent Analysis ◽  
Extracellular Electron Transfer ◽  
Multiple Partner ◽  
Sulfate Reducing ◽  
Primary Mechanism ◽  
Anaerobic Methanotrophs ◽  
Reducing Bacteria

ABSTRACT The anaerobic oxidation of methane by anaerobic methanotrophic (ANME) archaea in syntrophic partnership with deltaproteobacterial sulfate-reducing bacteria (SRB) is the primary mechanism for methane removal in ocean sediments. The mechanism of their syntrophy has been the subject of much research as traditional intermediate compounds, such as hydrogen and formate, failed to decouple the partners. Recent findings have indicated the potential for extracellular electron transfer from ANME archaea to SRB, though it is unclear how extracellular electrons are integrated into the metabolism of the SRB partner. We used metagenomics to reconstruct eight genomes from the globally distributed SEEP-SRB1 clade of ANME partner bacteria to determine what genomic features are required for syntrophy. The SEEP-SRB1 genomes contain large multiheme cytochromes that were not found in previously described free-living SRB and also lack periplasmic hydrogenases that may prevent an independent lifestyle without an extracellular source of electrons from ANME archaea. Metaproteomics revealed the expression of these cytochromes at in situ methane seep sediments from three sites along the Pacific coast of the United States. Phylogenetic analysis showed that these cytochromes appear to have been horizontally transferred from metal-respiring members of the Deltaproteobacteria such as Geobacter and may allow these syntrophic SRB to accept extracellular electrons in place of other chemical/organic electron donors. IMPORTANCE Some archaea, known as anaerobic methanotrophs, are capable of converting methane into carbon dioxide when they are growing syntopically with sulfate-reducing bacteria. This partnership is the primary mechanism for methane removal in ocean sediments; however, there is still much to learn about how this syntrophy works. Previous studies have failed to identify the metabolic intermediate, such as hydrogen or formate, that is passed between partners. However, recent analysis of methanotrophic archaea has suggested that the syntrophy is formed through direct electron transfer. In this research, we analyzed the genomes of multiple partner bacteria and showed that they also contain the genes necessary to perform extracellular electron transfer, which are absent in related bacteria that do not form syntrophic partnerships with anaerobic methanotrophs. This genomic evidence shows a possible mechanism for direct electron transfer from methanotrophic archaea into the metabolism of the partner bacteria. IMPORTANCE Some archaea, known as anaerobic methanotrophs, are capable of converting methane into carbon dioxide when they are growing syntopically with sulfate-reducing bacteria. This partnership is the primary mechanism for methane removal in ocean sediments; however, there is still much to learn about how this syntrophy works. Previous studies have failed to identify the metabolic intermediate, such as hydrogen or formate, that is passed between partners. However, recent analysis of methanotrophic archaea has suggested that the syntrophy is formed through direct electron transfer. In this research, we analyzed the genomes of multiple partner bacteria and showed that they also contain the genes necessary to perform extracellular electron transfer, which are absent in related bacteria that do not form syntrophic partnerships with anaerobic methanotrophs. This genomic evidence shows a possible mechanism for direct electron transfer from methanotrophic archaea into the metabolism of the partner bacteria.

scholarly journals Necessity of electrically conductive pili for methanogenesis with magnetite stimulation

PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e4541 ◽  
Author(s):  
Oumei Wang ◽  
Shiling Zheng ◽  
Bingchen Wang ◽  
Wenjing Wang ◽  
Fanghua Liu
Keyword(s):  
Electron Transfer ◽  
Methane Production ◽  
High Performance ◽  
Ethanol Metabolism ◽  
Electrically Conductive ◽  
Interspecies Electron Transfer ◽  
Transmission Electron ◽  
Anaerobic Soils ◽  
Soils And Sediments ◽  
Stimulation Of

Background Magnetite-mediated direct interspecies electron transfer (DIET) between Geobacter and Methanosarcina species is increasingly being invoked to explain magnetite stimulation of methane production in anaerobic soils and sediments. Although magnetite-mediated DIET has been documented in defined co-cultures reducing fumarate or nitrate as the electron acceptor, the effects of magnetite have only been inferred in methanogenic systems. Methods Concentrations of methane and organic acid were analysed with a gas chromatograph and high-performance liquid chromatography, respectively. The concentration of HCl-extractable Fe(II) was determined by the ferrozine method. The association of the defined co-cultures of G. metallireducens and M. barkeri with magnetite was observed with transmission electron micrographs. Results Magnetite stimulated ethanol metabolism and methane production in defined co-cultures of G. metallireducens and M. barkeri; however, magnetite did not promote methane production in co-cultures initiated with a culture of G. metallireducens that could not produce electrically conductive pili (e-pili), unlike the conductive carbon materials that facilitate DIET in the absence of e-pili. Transmission electron microscopy revealed that G. metallireducens and M. barkeri were closely associated when magnetite was present, as previously observed in G. metallireducens/G. sulfurreducens co-cultures. These results show that magnetite can promote DIET between Geobacter and Methanosarcina species, but not as a substitute for e-pili, and probably functions to facilitate electron transfer from the e-pili to Methanosarcina. Conclusion In summary, the e-pili are necessary for the stimulation of not only G. metallireducens/G. sulfurreducens, but also methanogenic G. metallireducens/M. barkeri co-cultures with magnetite.

scholarly journals Cytochrome OmcS is not essential for long-range electron transport in Geobacter sulfurreducens strain KN400

2020 ◽  
Author(s):  
David J. F. Walker ◽  
Yang Li ◽  
David Meier ◽  
Samantha Pinches ◽  
Dawn E. Holmes ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Electron Transport ◽  
Long Range ◽  
Geobacter Sulfurreducens ◽  
Extracellular Electron Transfer ◽  
Electrically Conductive ◽  
Closely Related Species ◽  
Direct Interspecies Electron Transfer ◽  
Interspecies Electron Transfer ◽  
Extracellular Electron Transport

AbstractThe multi-heme c-type cytochrome OmcS, is one of the central components for extracellular electron transport in Geobacter sulfurreducens strain DL-1, but its role in other microbes, including other strains of G. sulfurreducens is currently a matter of debate. Therefore, we investigated the function of OmcS in G. sulfurreducens strain KN400, which is even more effective in extracellular electron transfer than strain DL-1. We found that deleting omcS from strain KN400 did not negatively impact the rate of Fe(III) oxide reduction and did not affect the strain’s ability to accept electrons via direct interspecies electron transfer. The OmcS-deficient strain also continued to produce conductive filaments, consistent with the concept that electrically conductive pili are the primary conduit for long-range electron transfer in G. sulfurreducens and closely related species. These findings, coupled with the lack of OmcS homologs in most other microbes capable of extracellular electron transfer, suggest that OmcS is not a common critical component for extracellular electron transfer.

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