Electrically Conductive Biofilms Assembled by Magnetite in Anaerobic Oxidation of Methane Coupled to Debromination/Denitrification

Direct interspecies electron transfer (DIET) in syntrophic consortia comprised of anaerobic methanotrophic (ANME) archaea or methanogens and their electron-accepting partners is enigmatic since the identification of DIET just via gene expression for electrically conductive filaments (e-filaments) or membrane-bound multiheme c-type cytochromes (MHCs) is currently incredible. Additional evidence from electrochemical perspectives are desired. The study presented here showed that, in the presence of magnetite, biofilms, on hollow fiber membranes of a membrane biofilm reactor, comprised of ANME archaea/methanogens with their bromate-/nitrate-reducing partners were electrically active, based on electrochemical Fourier transform infrared spectra. Biofilms assembled by magnetite exhibited considerably high conductivity that was an order of magnitude higher than that without magnetite. High biofilm conductivity lowered the charge-transfer resistance within cell-to-cell electron exchange. Close examination of electrostatic force microscopy images observed the potential interspecies-connected networks assembled by filaments, along which magnetite was localized. Combining with evidence that most of the bands in Raman spectra related to c-type cytochromes faded out, it was suggested that magnetite mediated DIET between ANME archaea/methanogens and bromate-/nitrate-reducing bacteria via replacing a proposed function of MHCs. As a result, anaerobic oxidation of methane coupled to the simultaneous reduction of two electron acceptors, bromate and nitrate, was promoted.