scholarly journals Extracellular Electron Uptake by TwoMethanosarcinaSpecies

2018 ◽  
Author(s):  
Mon Oo Yee ◽  
Oona Snoeyenbos-West ◽  
Bo Thamdrup ◽  
Lars DM Ottosen ◽  
Amelia-Elena Rotaru
Keyword(s):  
Value Added ◽  
Surface Proteins ◽  
Redox Potentials ◽  
Electrically Conductive ◽  
Geobacter Metallireducens ◽  
Direct Interspecies Electron Transfer ◽  
Interspecies Electron Transfer ◽  
Relevant Group ◽  
Surface Redox ◽  
Conductive Particles

AbstractDirect electron uptake by prokaryotes is a recently described mechanism with a potential application for energy and CO2storage into value added chemicals. Members of Methanosarcinales, an environmentally and biotechnologically relevant group of methanogens, were previously shown to retrieve electrons from an extracellular electrogenic partner performing Direct Interspecies Electron Transfer (DIET) and were therefore proposed to be electroactive. However, their intrinsic electroactivity has never been examined. In this study, we tested two methanogens belonging to the genusMethanosarcina, M. barkeriandM. horonobensis,regarding their ability to accept electrons directly from insoluble electron donors like other cells, conductive particles and electrodes. Both methanogens were able to retrieve electrons fromGeobacter metallireducensvia DIET. Furthermore, DIET was also stimulated upon addition of electrically conductive granular activated carbon (GAC) when each was co-cultured withG. metallireducens. However, when provided with a cathode poised at −400 mV (vs. SHE), onlyM. barkericould perform electromethanogenesis. In contrast, the strict hydrogenotrophic methanogen,Methanobacterium formicicum, did not produce methane regardless of the type of insoluble electron donor provided (Geobactercells, GAC or electrodes). A comparison of functional gene categories between the twoMethanosarcinashowed differences regarding energy metabolism, which could explain dissimilarities concerning electromethanogenesis at fixed potentials. We suggest that these dissimilarities are minimized in the presence of an electrogenic DIET partner (e.g.Geobacter), which can modulate its surface redox potentials by adjusting the expression of electroactive surface proteins.

scholarly journals Direct Interspecies Electron Transfer between Geobacter metallireducens and Methanosarcina barkeri

2014 ◽  
Vol 80 (15) ◽  
pp. 4599-4605 ◽  
Author(s):  
Amelia-Elena Rotaru ◽  
Pravin Malla Shrestha ◽  
Fanghua Liu ◽  
Beatrice Markovaite ◽  
Shanshan Chen ◽  
...  
Keyword(s):  
Electron Transfer ◽  
Model Organism ◽  
Methanosarcina Barkeri ◽  
Physical Contact ◽  
Acetate Metabolism ◽  
Geobacter Metallireducens ◽  
Content Type ◽  
Direct Interspecies Electron Transfer ◽  
Interspecies Electron Transfer ◽  
Effective Form

ABSTRACTDirect interspecies electron transfer (DIET) is potentially an effective form of syntrophy in methanogenic communities, but little is known about the diversity of methanogens capable of DIET. The ability ofMethanosarcina barkerito participate in DIET was evaluated in coculture withGeobacter metallireducens. Cocultures formed aggregates that shared electrons via DIET during the stoichiometric conversion of ethanol to methane. Cocultures could not be initiated with a pilin-deficientG. metallireducensstrain, suggesting that long-range electron transfer along pili was important for DIET. Amendments of granular activated carbon permitted the pilin-deficientG. metallireducensisolates to share electrons withM. barkeri, demonstrating that this conductive material could substitute for pili in promoting DIET. WhenM. barkeriwas grown in coculture with the H2-producingPelobacter carbinolicus, incapable of DIET,M. barkeriutilized H2as an electron donor but metabolized little of the acetate thatP. carbinolicusproduced. This suggested that H2, but not electrons derived from DIET, inhibited acetate metabolism.P. carbinolicus-M. barkericocultures did not aggregate, demonstrating that, unlike DIET, close physical contact was not necessary for interspecies H2transfer.M. barkeriis the second methanogen found to accept electrons via DIET and the first methanogen known to be capable of using either H2or electrons derived from DIET for CO2reduction. Furthermore,M. barkeriis genetically tractable, making it a model organism for elucidating mechanisms by which methanogens make biological electrical connections with other cells.

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.

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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