A coupled function of biochar as geobattery and geoconductor leads to stimulation of microbial Fe(III) reduction and methanogenesis in a paddy soil enrichment culture

Abstract

Biochar can participate in biogeochemical electron transfer processes due to its electron-accepting and donating capabilities (i.e., geobattery) and electron conductivity (i.e., geoconductor). These two functions were separately demonstrated to play a role in biogeochemical iron cycling and methane formation. Yet, little is known about the coupled effect of both electron transfer mechanisms, even though naturally occurring electron transfer through biochar is expected to simultaneously rely on both geobattery and geoconductor mechanisms. Here, we incubated an anoxic paddy soil enrichment culture with acetate as the substrate to investigate how biochar's coupled electron transfer mechanisms influence the electron transfer pathways between microbes and Fe(III) minerals and how it impacts the soil microbial community composition. We found that biochar simultaneously stimulated microbial Fe(III) reduction and methanogenesis by 2.6 and 2.3 fold, but these processes were spatially decoupled. Small biochar particles (5–20 μm) caused higher Fe(III) reduction and methanogenesis rates than large particles (50–100 μm). The addition of biochar enriched a syntrophic acetate-oxidizing co-culture with dominating Fe(III)-reducing Geobacteraceae taxa and acetoclastic methanogenic Methanosarcina taxa. After acetoclastic methanogenesis stopped, the observed continuing methanogenesis was likely due to interspecies electron transfer caused by biochar functioning as a geoconductor transferring electrons from Geobacteraceae to Methanosarcina. In summary, the simultaneous occurrence of Fe(III) reduction and methanogenesis leads to the formation of a cell-biochar-mineral battery network and a cell-biochar-cell conductive network in an enrichment culture from a paddy soil.