Ecological and genomic profiling of anaerobic methane-oxidizing archaea in a deep granitic environment

Abstract

Recent single-gene-based surveys of deep continental aquifers demonstrated the widespread occurrence of archaea related to Candidatus Methanoperedens nitroreducens (ANME-2d) known to mediate anaerobic oxidation of methane (AOM). However, it is unclear whether ANME-2d mediates AOM in the deep continental biosphere. In this study, we found the dominance of ANME-2d in groundwater enriched in sulfate and methane from a 300-m deep underground borehole in granitic rock. A near-complete genome of one representative species of the ANME-2d obtained from the underground borehole has most of functional genes required for AOM and assimilatory sulfate reduction. The genome of the subsurface ANME-2d is different from those of other members of ANME-2d by lacking functional genes encoding nitrate and nitrite reductases and multiheme cytochromes. In addition, the subsurface ANME-2d genome contains a membrane-bound NiFe hydrogenase gene putatively involved in respiratory H oxidation, which is different from those of other methanotrophic archaea. Short-term incubation of microbial cells collected from the granitic groundwater with C-labeled methane also demonstrates that AOM is linked to microbial sulfate reduction. Given the prominence of granitic continental crust and sulfate and methane in terrestrial subsurface fluids, we conclude that AOM may be widespread in the deep continental biosphere.

Energetic and Environmental Constraints on the Community Structure of Benthic Microbial Mats in Lake Fryxell, Antarctica

“…The relationships between communities and environmental characteristics have historically been studied in the presence of macroflora and -fauna because there are few places on Earth where microbial niches are not at least partly structured by macroorganisms. Some of these environments include hot springs (Amin et al 2017) , the deep biosphere (Ino et al 2018) , and snowfall (Brown and Jumpponen 2019) , and studies of them have been foundational to evaluating the application of ecological principles to microbial ecosystems .…”

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

“…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). In order to recover additional genomes belonging to the family, GraftM (32) was used to screen public metagenome sequence datasets from NCBI for Methanoperedenaceae -related 16S rRNA and mcrA gene sequences.…”

“…The use of hydrogen (H 2 ; E 0 = −414mV (39)) as an electron source was previously suggested for MGW-1 and HGW-1 which encode Group 1 membrane-bound NiFe hydrogenase complexes, composed of a NiFe catalytic subunit, a FeS electron transfer subunit, and a membrane-bound b -type cytochrome (29, 30). These hydrogenases, along with similar Group 1 NiFe hydrogenases identified in the ASW-6 and CMD-2 MAGs, form a monophyletic clade with those encoded by the MAG for “ Ca .…”

“…The MGW-1 (ref. 29) and ASW-2 MAGs also encode Group 3b hydrogenases which have been implicated in hydrogen evolution and nicotinamide adenine dinucleotide phosphate (NADPH) reduction (42). Similar complexes have also been shown to have hydrogen oxidation and elemental sulfur reducing capabilities (42–44).…”

“…MGW-1 was recently speculated to directly couple AOM to sulfate reduction utilising assimilatory sulfate reduction pathways. This hypothesis was based on the lack of large MHCs or identifiable alternate electron acceptor complexes encoded in the MAG (29). Several of the Methanoperedenaceae MAGs, and those of other ANME lineages, contain candidate genes associated with assimilatory sulfate reduction, but a dissimilatory role for these has not been shown (68).…”