A methanotrophic archaeon couples anaerobic oxidation of methane to Fe(III) reduction

Abstract

Microbially mediated anaerobic oxidation of methane (AOM) is a key process in the regulation of methane emissions to the atmosphere. Iron can serve as an electron acceptor for AOM, and it has been suggested that Fe(III)-dependent AOM potentially comprises a major global methane sink. Although it has been proposed that anaerobic methanotrophic (ANME) archaea can facilitate this process, their active metabolic pathways have not been confirmed. Here we report the enrichment and characterisation of a novel archaeon in a laboratory-scale bioreactor fed with Fe(III) oxide (ferrihydrite) and methane. Long-term performance data, in conjunction with the C- andFe-labelling batch experiments, demonstrated that AOM was coupled to Fe(III) reduction to Fe(II) in this bioreactor. Metagenomic analysis showed that this archaeon belongs to a novel genus within family Candidatus Methanoperedenaceae, and possesses genes encoding the "reverse methanogenesis" pathway, as well as multi-heme c-type cytochromes which are hypothesised to facilitate dissimilatory Fe(III) reduction. Metatranscriptomic analysis revealed upregulation of these genes, supporting that this archaeon can independently mediate AOM using Fe(III) as the terminal electron acceptor. We propose the name Candidatus "Methanoperedens ferrireducens" for this microorganism. The potential role of "M. ferrireducens" in linking the carbon and iron cycles in environments rich in methane and iron should be investigated in future research.

Manganese/iron-supported sulfate-dependent anaerobic oxidation of methane by archaea in lake sediments

“…Moreover, it remains unclear whether microorganisms in environments where both 69 independently mediate AOM using iron or manganese oxides (i.e., Fe(III)/Mn(IV)) as 71 the terminal electron acceptors (Ettwig et al 2016;Cai et al 2018), or whether 72 canonical sulfate-dependent AOM is indirectly stimulated by metal oxides that drive 73 sulfide/sulfur oxidation via a cryptic sulfur cycle (Holmkvist et al 2011a;Hansel et 74 al. 2015).…”

Rates and pathways of CH4 oxidation in ferruginous Lake Matano, Indonesia

“…In some cases, SO 4 is present, but AOM appears partially or entirely decoupled from sulfate reduction (Beal, House, & Orphan, 2009;Gupta et al, 2013;Segarra, Comerford, Slaughter, & Joye, 2013;Segarra et al, 2015;Sivan, Antler, Turchyn, Marlow, & Orphan, 2014). Despite the growing number of reports on Fe-dependent CH 4 oxidation (Bar-Or et al, 2017;Cai et al, 2018;Egger et al, 2015;Ettwig et al, 2016;Fu et al, 2016;Gao et al, 2017;Nordi et al, 2013;Roland et al, 2018;Scheller, Yu, Chadwick, Mcglynn, & Orphan, 2016), the pathway remains unsubstantiated through pure culture experiments and its broader ecological importance is as yet unknown. Lake Matano, Sulawesi Island, Indonesia, is situated near the equator and hosts the largest, deepest, and oldest known ferruginous basin on Earth (Crowe, Jones, et al, 2008;.…”

2038 – When microbes rule the Earth

“…The hunt for spookmicrobes generally starts with biogeochemical evidence, such as colocalized depletion, which could not be explained by physical processes, of two compounds that could react to generate energy, and may include stable-and radioisotopic evidence of microbial involvement. A classic example is the discovery of anaerobic methane oxidation (see In 0 t Zandt et al, 2018), for which we now know the microbes that couple the oxidation of methane to terminal electron acceptors such as sulfate, nitrate and nitrite, while the Archaea that use Fe(III) as terminal electron acceptor evaded identification until very recently (Cai et al, 2018). Genomic reconstruction of 'Candidatus Methylomirabilis oxyfera', the dominant member of a culture carrying out nitrite-dependent anaerobic oxidation of methane, has revealed a fascinating mechanism whereby it converts nitrite to nitric oxide, which is dismutated to nitrogen and oxygen, and the latter is then used to oxidize methane by the well-known aerobic pathway (Ettwig et al 2010).…”