Insights into the biochar-respiratory growth of a model methanogen

Abstract

Abstract Biochar is ubiquitous in diverse natural and engineered anaerobic systems. The biogeochemical roles of biochar during its production, storage and dynamics show an involvement in the global methane flux that is governed by methanotrophs and methanogens. Understanding of the relevant mechanisms is currently restricted to the roles of biochar in the methanotrophic growth but less is known of the roles in methanogenic growth. Here, we demonstrated that biochar enhanced methanogenic growth of a model methanogen Methanosarcina acetivorans, and the role of biochar as an electron acceptor during the methanogenic growth was confirmed, referring as biochar-respiratory growth. The biochar-respiratory growth of M. acetivorans promoted the secretion of extracellular polymeric substances (EPS) with augmented electron transfer capability, and the removal of EPS significantly attenuated extracellular electron transfer. Identification and quantification of prosthetic cofactors for EPS suggest an important role of flavin and F420 in the extracellular electron transfer. Transcriptomic analysis provided more insights into the biochar-respiratory growth of M. acetivorans to show that transcriptional regulation positively responded to the favorable growth environment provided by biochar, thereby stimulating global methanogenesis. Our results enlighten the in situ roles of biochar in the ecophysiology of methanogens in diverse anaerobic environments.