Enhanced methanogenesis in acidic fen peatlands via ferrihydrite reduction-driven microbial metabolisms

Wang H.Y.; Hu X.Y.; Zhou F.W.; Hernandez J.C.; Yu Z.G.; Dorodnikov M.; Knorr K.H.; Kappler A.

Abstract

Interactions between Fe(III) reduction and methanogenesis in regulating CH4 emissions remain controversial, particularly in peatlands. To address this, we investigated the effects of ferrihydrite amendments on net CH4 formation in four moderately acidic fen soils from the Great Khingan Mountains, the Changbai Mountains, the Tibetan Plateau, and Dajiuhu. Anaerobic microcosms were established to monitor gas formation and porewater chemistry, while detailed geochemical and microbiome profiling was conducted for the soils from the Changbai Mountains. Ferrihydrite additions increased net CH4 formation rates by 1.4–6.2 times, with stronger effects observed in soils with more available carbon. As expected, secondary crystalline magnetite did not form. Ferrihydrite reduction mainly occurred during the pre-methanogenic stage and was mediated by fermentative Fe(III)-reducing bacteria, such as Clostridium and OPB41 . These microbes lowered H2 levels, reducing the relative abundance of Methanobacterium from 86% to 56%. However, fermentative Fe(III) reduction mitigated limitations on organic matter decomposition by elevating pH and improving the thermodynamic feasibility of organic carbon fermentation in the pre-methanogenic stage. Beyond enhanced substrate supply, the legacy of elevated pH further promoted activities of acetoclastic methanogens, as indicated by faster net acetate consumption in ferrihydrite treatments. Enriched metagenome-assembled genomes (MAGs) affiliated with Sumerlaeaceae , Clostridium , OPB41 , and Prolixibacteraceae revealed the potential for polysaccharide hydrolysis and acetogenesis. Most of the enriched acetogens engaged in syntrophic interactions with methanogens. Collectively, our findings suggest that fermentative Fe(III) reduction can stimulate organic matter decomposition, while its legacy of elevated pH further accelerates organic matter decomposition and methanogenesis in acidic peatland soils.