Enhancement of methanogenesis by electric syntrophy with biogenic iron‐sulfide minerals

Abstract

Recent studies have shown that interspecies electron transfer between chemoheterotrophic bacteria and methanogenic archaea can be mediated by electric currents flowing through conductive iron oxides, a process termed electric syntrophy. In this study, we conducted enrichment experiments with methanogenic microbial communities from rice paddy soil in the presence of ferrihydrite and/or sulfate to determine whether electric syntrophy could be enabled by biogenic iron sulfides. Although supplementation with either ferrihydrite or sulfate alone suppressed methanogenesis, supplementation with both ferrihydrite and sulfate enhanced methanogenesis. In the presence of sulfate, ferrihydrite was transformed into black precipitates consisting mainly of poorly crystalline iron sulfides. Microbial community analysis revealed that a methanogenic archaeon and iron- and sulfate-reducing bacteria (Methanosarcina, Geobacter, and Desulfotomaculum, respectively) predominated in the enrichment culture supplemented with both ferrihydrite and sulfate. Addition of an inhibitor specific for methanogenic archaea decreased the abundance of Geobacter, but not Desulfotomaculum, indicating that Geobacter acquired energy via syntrophic interaction with methanogenic archaea. Although electron acceptor compounds such as sulfate and iron oxides have been thought to suppress methanogenesis, this study revealed that coexistence of sulfate and iron oxide can promote methanogenesis by biomineralization of (semi)conductive iron sulfides that enable methanogenesis via electric syntrophy.

Branched Medium Chain Fatty Acids: Iso-Caproate Formation from Iso-Butyrate Broadens the Product Spectrum for Microbial Chain Elongation

“…69,70 Some types of FeS compounds have been shown to enhance direct interspecies electron transfer. 59…”

Benefits at the nanoscale: a review of nanoparticle‐enabled processes favouring microbial growth and functionality

“…Nanoparticle‐assisted electron transfer is particularly important for methanogenesis that relies on close interactions between Bacteria and Archaea ; theoretical calculations indicate that interspecies electron flux via nanoparticles is about 10 6 times higher than using diffusible H 2 molecules (Cruz Viggi et al ., 2014). Consistent with this calculation, methane‐producing microbial communities enriched from paddy soils, anaerobic digesters and lake and coastal sediments display 0.3 to 4 times faster methane production rates when conductive nanoparticles are added to the cultures (Kato et al ., 2012a; Yamada et al ., 2015; Zhuang et al ., 2015, 2018; Kato and Igarashi, 2018; Rotaru et al ., 2018, 2019). In one particular case, methanogenesis was only sustainable in the presence of conductive nanoparticles (Rotaru et al ., 2019).…”

Methanogenic Activity and Microbial Community Structure in Response to Different Mineralization Pathways of Ferrihydrite in Paddy Soil

“…Each secondary product has its own unique characteristics (such as crystal structure, particle size, redox potential, and conductivity), which determine its specific impact on the related biogeochemical processes. Recently, there are increasing studies investigating the association between biomineralization of iron (hydr)oxides and microbial methanogenesis (Jiang et al, 2013;Zhuang et al, 2015b;Zheng et al, 2017;Kato and Igarashi, 2019); biogenic magnetite and iron sulfides are demonstrated to enhance methanogenesis in soil and sediment. As the first attempt, our previous study (Tang et al, 2016) investigated the response of methanogenic activity to different transformation pathways of ferrihydrite in the artificial coculture of Geobacter and Methanosarcina.…”