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

Abstract

Reactive Fe(III) minerals can influence methane (CH ) emissions by inhibiting microbial methanogenesis or by stimulating anaerobic CH oxidation. The balance between Fe(III) reduction, methanogenesis, and CH oxidation in ferruginous Archean and Paleoproterozoic oceans would have controlled CH fluxes to the atmosphere, thereby regulating the capacity for CH to warm the early Earth under the Faint Young Sun. We studied CH and 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, CH oxidation, 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 CH production 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 CH oxidation, although some incubations displayed CH -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 CH as a greenhouse gas throughout the first half of Earth history.

Biogeochemical and physical controls on methane fluxes from two ferruginous meromictic lakes

“…The overwhelming majority of recovered methanogen sequence reads in both water columns belong to hydrogenotrophic organisms as opposed to acetoclastic organisms, yet the C‐ and H‐isotopic composition of CH 4 implies a mixture of the two (Table S3). Hydrogenotrophic methanogenesis under ferruginous conditions is consistent with prior studies (see Bray et al, ). The persistence of Fe(III) oxides to sediment has also been observed in other seasonally stratified ferruginous lakes (Davison, ).…”

Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures

“…1b, 4). Enhanced iron reduction with the more reactive lepidocrocite likely resulted in the inhibition of methanogenesis; a phenomenon previously demonstrated when ferrihydrite was provided to ferruginous lake sediments incubations [53]. However, unlike the sediment incubation with lepidocrocite where iron reduction reached a plateau before methanogenesis onset (Fig.…”

Iron formations: A global record of Neoarchaean to Palaeoproterozoic environmental history

“…Li et al, 2013a), the presence of Fe(II)-bearing minerals in IF (e.g., magnetite, siderite, greenalite -recall section 2.3), and the general lack of microfossils preserved in the Fe-rich layers lacking silicification. Moreover, the reduction of ferric iron may also have been coupled to the anaerobic oxidation of methane , an observation supported by the reaction's likely occurrence in modern marine sediments (Riedinger et al, 2014) and lakes (Crowe et al, 2011), as well as in culture experiments (Ettwig et al, 2016;Bray et al, 2017). …”