Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae

Abstract

Anaerobic oxidation of methane (AOM) is a major biological process that reduces global methane emission to the atmosphere. Anaerobic methanotrophic archaea (ANME) mediate this process through the coupling of methane oxidation to different electron acceptors, or in concert with a syntrophic bacterial partner. Recently, ANME belonging to the archaeal family Methanoperedenaceae (formerly known as ANME-2d) were shown to be capable of AOM coupled to nitrate and iron reduction. Here, a freshwater sediment bioreactor fed with methane and Mn(IV) oxides (birnessite) resulted in a microbial community dominated by two novel members of the Methanoperedenaceae, with biochemical profiling of the system demonstrating Mn(IV)-dependent AOM. Genomic and transcriptomic analyses revealed the expression of key genes involved in methane oxidation and several shared multiheme c-type cytochromes (MHCs) that were differentially expressed, indicating the likely use of different extracellular electron transfer pathways. We propose the names "Candidatus Methanoperedens manganicus" and "Candidatus Methanoperedens manganireducens" for the two newly described Methanoperedenaceae species. This study demonstrates the ability of members of the Methanoperedenaceae to couple AOM to the reduction of Mn (IV) oxides, which suggests their potential role in linking methane and manganese cycling in the environment. Etymology "Candidatus Methanoperedens manganicus" sp. nov "Candidatus Methanoperedens manganireducens" sp. nov "Candidatus Methanoperedens manganicus": man.

Lateral gene transfer drives metabolic flexibility in the anaerobic methane oxidising archaeal family Methanoperedenaceae

“…Methanoperedens manganicus” and “ Ca . Methanoperedens manganireducens”, Mn-1 and Mn-2, respectively (12)). Also included are two environmental MAGs recovered from groundwater samples from the Horonobe and Mizunami underground research laboratories in Japan (HGW-1 and MGW-1) (29, 30), and one MAG from an Italian paddy soil sample (IPS-1) (31).…”

“…Different lineages of anaerobic methanotrophic (ANME) archaea are hypothesised to mediate AOM through the reversal of the methanogenesis pathway and conserve energy using mechanisms similar to those found in methylotrophic and aceticlastic methanogens (6). Unlike methanogens, most of these ANMEs encode a large repertoire of multi-heme c -type cytochromes (MHCs), which are proposed to mediate direct interspecies electron transfer to syntrophic sulfate-reducing bacteria (SRB)(7, 8), and/or the reduction of metal oxides and humic acids (9–12).…”

“…M nitroreducens”, potentially allowing these microorganisms to coupled AOM to dissimilatory nitrate reduction to ammonia (DNRA) (24). More recently, three novel species belonging to the Methanoperedenaceae were enriched in bioreactors demonstrated to couple AOM to the reduction of insoluble iron or manganese oxides (9, 12). These microorganisms did not encode dissimilatory nitrate reduction pathways, but instead were inferred to use multiple unique MHCs during metal-dependent AOM to facilitate the transfer of electrons to the metal oxides (9, 12), consistent with the extracellular electron transfer mechanisms proposed for marine ANME (7, 8).…”

“…More recently, three novel species belonging to the Methanoperedenaceae were enriched in bioreactors demonstrated to couple AOM to the reduction of insoluble iron or manganese oxides (9, 12). These microorganisms did not encode dissimilatory nitrate reduction pathways, but instead were inferred to use multiple unique MHCs during metal-dependent AOM to facilitate the transfer of electrons to the metal oxides (9, 12), consistent with the extracellular electron transfer mechanisms proposed for marine ANME (7, 8). Bioreactor performance and 16S rRNA gene amplicon data has also been used to suggest that members of the Methanoperedenaceae are capable of AOM coupled to the reduction of selenate and chromium(VI), although this remains to be confirmed with more direct evidence (25, 26).…”

Thermogenic hydrocarbons fuel a redox stratified subseafloor microbiome in deep sea cold seep sediments

“…Numerous studies have focused on anaerobic oxidation of methane, since methane generally is the dominant hydrocarbon in cold seep fluids. This process is mediated by anaerobic methanotrophic archaea (ANME) through the reverse methanogenesis pathway, typically in syntrophy with bacteria that can reduce electron acceptors such as sulfate, nitrate, and metal oxides 8, 15, 16 . Investigations of enrichment cultures have also revealed anaerobic bacterial or archaeal oxidation of non-methane alkanes and aromatic hydrocarbons, including ethane (e.g.…”