Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri

• Published in: Applied and environmental microbiology 2014-08, Vol.80 (15), p.4599-4605
• Main Authors: Rotaru, Amelia-Elena, Shrestha, Pravin Malla, Liu, Fanghua, Markovaite, Beatrice, Chen, Shanshan, Nevin, Kelly P, Lovley, Derek R
• Format: Article
• Language: English
• Subjects: Bacteria; Biological Transport; Cells; Electron transfer; Electron Transport; Electrons; Environmental Microbiology; Ethanol; Ethanol - metabolism; Fimbriae Proteins - genetics; Fimbriae Proteins - metabolism; Fimbriae, Bacterial - genetics; Fimbriae, Bacterial - metabolism; Geobacter - genetics; Geobacter - metabolism; Geobacter metallireducens; Hydrogen - metabolism; Metabolism; Methane; Methane - metabolism; Methanosarcina barkeri; Methanosarcina barkeri - genetics; Methanosarcina barkeri - metabolism
• ISSN: 0099-2240; 1098-5336
• DOI: 10.1128/aem.00895-14

Direct 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 of Methanosarcina barkeri to participate in DIET was evaluated in coculture with Geobacter 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-deficient G. metallireducens strain, suggesting that long-range electron transfer along pili was important for DIET. Amendments of granular activated carbon permitted the pilin-deficient G. metallireducens isolates to share electrons with M. barkeri, demonstrating that this conductive material could substitute for pili in promoting DIET. When M. barkeri was grown in coculture with the H2-producing Pelobacter carbinolicus, incapable of DIET, M. barkeri utilized H2 as an electron donor but metabolized little of the acetate that P.carbinolicus produced. This suggested that H2, but not electrons derived from DIET, inhibited acetate metabolism. P. carbinolicus-M. barkeri cocultures did not aggregate, demonstrating that, unlike DIET, close physical contact was not necessary for interspecies H2 transfer. M. barkeri is the second methanogen found to accept electrons via DIET and the first methanogen known to be capable of using either H2 or electrons derived from DIET for CO2 reduction. Furthermore, M. barkeri is genetically tractable,making it a model organism for elucidating mechanisms by which methanogens make biological electrical connections with other cells.