Formate-derived H2, a driver of hydrogenotrophic processes in the root-zone of a methane-emitting fen

Summary Wetlands are important sources of globally emitted methane. Plants mediate much of that emission by releasing root‐derived organic carbon, including formate, a direct precursor of methane. Thus, the objective of this study was to resolve formate‐driven processes potentially linked to methanogenesis in the fen root‐zone. Although, formate was anticipated to directly trigger methanogenesis, the rapid anaerobic consumption of formate by Carex roots unexpectedly yielded H2 and CO2 via enzymes such as formate‐H2‐lyase (FHL), and likewise appeared to enhance the utilization of organic carbon. Collectively, 57 [FeFe]‐ and [NiFe]‐hydrogenase‐containing family level phylotypes potentially linked to FHL activity were detected. Under anoxic conditions, root‐derived fermentative Citrobacter and Hafnia isolates produced H2 from formate via FHL. Formate‐derived H2 fueled methanogenesis and acetogenesis, and methanogenic (Methanoregula, Methanobacterium, Methanocella) and acetogenic (Acetonema, Clostridum, Sporomusa) genera potentially linked to these hydrogenotrophic activities were identified. The findings (i) provide novel insights on highly diverse root‐associated FHL‐containing taxa that can augment secondary hydrogenotrophic processes via the production of formate‐derived H2, (ii) demonstrate that formate can have a ‘priming’ effect on the utilization of organic carbon, and (iii) raise questions regarding the fate of formate‐derived H2 when it diffuses away from the root‐zone.