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

Hunger, Sindy, Schmidt, Oliver, Gößner, Anita S., Drake, Harold L.
Environmental microbiology 2016 v.18 no.9 pp. 3106-3119
Acetonema, Carex, Citrobacter, Hafnia, Methanobacterium, Sporomusa, anaerobic conditions, carbon dioxide, enzymes, formates, hydrogen, methane, methane production, methanogens, organic carbon, phylotype, rhizosphere, roots, wetlands
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.