Shifting microbial communities sustain multiyear iron reduction and methanogenesis in ferruginous sediment incubations

Abstract

© 2017 John Wiley & Sons Ltd Reactive Fe(III) minerals can influence methane (CH4) emissions by inhibiting microbial methanogenesis or by stimulating anaerobic CH4oxidation. The balance between Fe(III) reduction, methanogenesis, and CH4oxidation in ferruginous Archean and Paleoproterozoic oceans would have controlled CH4fluxes to the atmosphere, thereby regulating the capacity for CH4to warm the early Earth under the Faint Young Sun. We studied CH4and Fe cycling in anoxic incubations of ferruginous sediment from the ancient ocean analogue Lake Matano, Indonesia, over three successive transfers (500 days in total). Iron reduction, methanogenesis, CH4oxidation, and microbial taxonomy were monitored in treatments amended with ferrihydrite or goethite. After three dilutions, Fe(III) reduction persisted only in bottles with ferrihydrite. Enhanced CH4production was observed in the presence of goethite, highlighting the potential for reactive Fe(III) oxides to inhibit methanogenesis. Supplementing the media with hydrogen, nickel and selenium did not stimulate methanogenesis. There was limited evidence for Fe(III)-dependent CH4oxidation, although some incubations displayed CH4-stimulated Fe(III) reduction. 16S rRNA profiles continuously changed over the course of enrichment, with ultimate dominance of unclassified members of the order Desulfuromonadales in all treatments. Microbial diversity decreased markedly over the course of incubation, with subtle differences between ferrihydrite and goethite amendments. These results suggest that Fe(III) oxide mineralogy and availability of electron donors could have led to spatial separation of Fe(III)-reducing and methanogenic microbial communities in ferruginous marine sediments, potentially explaining the persistence of CH4as a greenhouse gas throughout the first half of Earth history.