Potential of direct interspecies electron transfer in synergetic enhancement of methanogenesis and sulfate removal in an up-flow anaerobic sludge blanket reactor with magnetite

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.

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Engineering Enhanced Anaerobic Digestion: Benefits of Ethanol Fermentation Pretreatment for Boosting Direct Interspecies Electron Transfer

Energy ◽

10.1016/j.energy.2021.120643 ◽

2021 ◽

pp. 120643

Author(s):

Zhiqiang Zhao ◽

Yang Li ◽

Yaobin Zhang

Keyword(s):

Electron Transfer ◽

Anaerobic Digestion ◽

Ethanol Fermentation ◽

Direct Interspecies Electron Transfer ◽

Interspecies Electron Transfer

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Stimulation and inhibition of direct interspecies electron transfer mechanisms within methanogenic reactors by adding magnetite and granular actived carbon

Chemical Engineering Journal ◽

10.1016/j.cej.2021.128882 ◽

2021 ◽

Vol 415 ◽

pp. 128882

Author(s):

Willame A. Cavalcante ◽

Tito A. Gehring ◽

Marcelo Zaiat

Keyword(s):

Electron Transfer ◽

Direct Interspecies Electron Transfer ◽

Interspecies Electron Transfer ◽

Actived Carbon ◽

Transfer Mechanisms

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Direct Interspecies Electron Transfer between Geobacter metallireducens and Methanosarcina barkeri

Applied and Environmental Microbiology ◽

10.1128/aem.00895-14 ◽

2014 ◽

Vol 80 (15) ◽

pp. 4599-4605 ◽

Cited By ~ 398

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.

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