Deep-branching ANME-1c archaea grow at the upper temperature limit of anaerobic oxidation of methane

Abstract

In seafloor sediments, the anaerobic oxidation of methane (AOM) consumes most of the methane formed in anoxic layers, preventing this greenhouse gas from reaching the water column and finally the atmosphere. AOM is performed by syntrophic consortia of specific anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria (SRB). Cultures with diverse AOM partners exist at temperatures between 12°C and 60°C. Here, from hydrothermally heated sediments of the Guaymas Basin, we cultured deep-branching ANME-1c that grow in syntrophic consortia with Thermodesulfobacteria at 70°C. Like all ANME, ANME-1c oxidize methane using the methanogenesis pathway in reverse. As an uncommon feature, ANME-1c encode a nickel-iron hydrogenase. This hydrogenase has low expression during AOM and the partner Thermodesulfobacteria lack hydrogen-consuming hydrogenases. Therefore, it is unlikely that the partners exchange hydrogen during AOM. ANME-1c also does not consume hydrogen for methane formation, disputing a recent hypothesis on facultative methanogenesis. We hypothesize that the ANME-1c hydrogenase might have been present in the common ancestor of ANME-1 but lost its central metabolic function in ANME-1c archaea. For potential direct interspecies electron transfer (DIET), both partners encode and express genes coding for extracellular appendages and multiheme cytochromes. Thermodesulfobacteria encode and express an extracellular pentaheme cytochrome with high similarity to cytochromes of other syntrophic sulfate-reducing partner bacteria. ANME-1c might associate specifically to Thermodesulfobacteria, but their co-occurrence is so far only documented for heated sediments of the Gulf of California. However, in the deep seafloor, sulfate–methane interphases appear at temperatures up to 80°C, suggesting these as potential habitats for the partnership of ANME-1c and Thermodesulfobacteria.

Composition and Metabolic Potential of Fe(III)-Reducing Enrichment Cultures of Methanotrophic ANME-2a Archaea and Associated Bacteria

“…The gene of large hydrogenase subunit is a part of the cluster, which codes for uptake hydrogenase small subunit precursor (MCL7474639), four hydrogenase assembly proteins HypDEFC (MCL7474633-36) and hydrogenase maturation protease (MCL7474637). Genes for [FeFe] and [NiFe] hydrogenases were identified in ANME-1 and Methanoperedenaceae [ 23 , 57 , 63 , 64 ], but as far as we know, the presence of hydrogenases in the genomes of ANME-2 has not been reported previously. Our finding suggests that representatives of ANME-2 are potentially able to perform hydrogenotrophic methanogenesis.…”

“…This sulfate-reducing bacterium can be cultivated without ANME-1 using hydrogen as an electron donor [ 22 ]. Another thermophilic sulfate-reducing partner of ANME-1 at 70 °C is Candidatus Thermodesulfobacterium torris belonging to the class Thermodesulfobacteria [ 23 ]. Apart from “ Desulfobacterota” , other bacterial groups that have been found to be significantly correlated with ANME are Betaproteobacteria and Verrucomicrobia , but the factors that determine interactions between these bacteria and archaea are not clear [ 24 , 25 ].…”

PCR-based survey of methane-cycling archaea in methane-soaked subsurface sediments of Guaymas Basin, Gulf of California

“…In searching for thermophilic ANME-1 lineages, we found that cluster VIII, consisting of mcrA genes from ANME-1 enrichments in surficial sediments at 50°C [13], also included Guaymas subsurface mcrA genes from site U1551B. However, we observed no overlap of Guaymas subsurface mcrA genes with mcrA genes from thermophilic methane-oxidizing ANME-1 enrichment cultures that are active at 70°C [15, 17].…”

“…Sulfate-dependent anaerobic methane-oxidizing archaea (predominantly ANME-1 and ANME-2) are widespread in surficial sediments of Guaymas Basin (Teske et al, 2002, Biddle et al, 2012, Dowell et al, 2016, McKay et al, 2016). Thermophilic ANME-1 lineages were enriched from hydrothermal sediments of Guaymas Basin at temperatures ranging from 50 to 70°C (Holler et al 2011, Wegener et al 2015, Benito-Merino et al 2022), and at 70°C from Pescadero Basin in the southern Gulf of California (Speth et al 2022, Laso-Pérez et al 2023).…”

A comprehensive catalog with 100 million genes and 3,000 metagenome-assembled genomes from global cold seep sediments

“…Fortunately, in seep sediments, methane could be consumed through the process of anaerobic oxidation of methane (AOM). This process removes roughly 90% of the methane produced globally in marine sediments, acting as an efficient methane filter 3,4 .…”