Genomic and enzymatic evidence of acetogenesis by anaerobic methanotrophic archaea

Abstract

Anaerobic oxidation of methane (AOM) mediated by anaerobic methanotrophic archaea (ANME) is the primary process that provides energy to cold seep ecosystems by converting methane into inorganic carbon. Notably, cold seep ecosystems are dominated by highly divergent heterotrophic microorganisms. The role of the AOM process in supporting heterotrophic population remains unknown. We investigate the acetogenic capacity of ANME-2a in a simulated cold seep ecosystem using high-pressure biotechnology, where both AOM activity and acetate production are detected. The production of acetate from methane is confirmed by isotope-labeling experiments. A complete archaeal acetogenesis pathway is identified in the ANME-2a genome, and apparent acetogenic activity of the key enzymes ADP-forming acetate-CoA ligase and acetyl-CoA synthetase is demonstrated. Here, we propose a modified model of carbon cycling in cold seeps: during AOM process, methane can be converted into organic carbon, such as acetate, which further fuels the heterotrophic community in the ecosystem.

Distinct Bottom-Water Bacterial Communities at Methane Seeps With Various Seepage Intensities in Haima, South China Sea

“…We found apart from CH 4 , which acts as the key environmental variable shaping the bacterial community structure, DOC, nitrate, and ammonium concentrations also correlated statistically significantly with bacterial community abundances. Because CH 4 oxidation by autotrophic methanotrophs leads to DOC production (Yang et al, 2020), the effect of DOC on shaping the bacterial community may be caused by CH 4 variation. Moreover, as many oil-degrading bacteria are enriched at the LIS and HIS sites, there is also the possibility of oil seepage at these sites with DOC produced through oil biodegradation by these bacteria (Orcutt et al, 2010).…”

Hydrostatic pressure is the universal key driver of microbial evolution in the deep ocean and beyond

“…HHP may induce significant metabolic alterations within cells, as it alters the dissolved gas concentration and the intracellular oxidation status (Xie et al ., 2018; Yang et al ., 2020). The former impact is straightforward in that more gas is dissolved under elevated hydrostatic pressure.…”

Production of Labile Protein-Like Dissolved Organic Carbon Associated With Anaerobic Methane Oxidization in the Haima Cold Seeps, South China Sea

“…Although the exact formation mechanism of methane-derived DOC is currently unclear, biochemical processes including methane-sourced carbon incorporation into acetate or larger biomoleculars, microbial excretion, and biomass degradation have been proposed (Hoehler et al, 1994;Yang et al, 2020). Here, greater amount of fluorescent protein-like components (C2 and C4) and correspondingly less amount of humic-like components (C1 and C3) at the seep cores (ROV1, ROV5) than those at the reference core (QDN-C-S03) suggests enhanced microbial activities and resulting release of more labile, proteinlike components at the seep cores (Figure 3).…”

“…However, the correlation between the fluorescent intensity of the other protein-like component-C4 and DOC concentration as well as δ 13 C-DOC at both seep cores is less remarkable compared to C2, likely implying complicated sources and formation mechanism of C4. Although the specific chemical composition of methane-derived DOC has yet to be investigated, it has been suggested that methane could be converted to low-molecular-weight, labile organic materials (e.g., acetate) by AOM (Yang et al, 2020). This inference was demonstrated by the identification of a complete archaeal acetogenesis pathway in the ANME-2a genome and the activity of the key enzymes in acetate generation (Yang et al, 2020).…”

“…Although the specific chemical composition of methane-derived DOC has yet to be investigated, it has been suggested that methane could be converted to low-molecular-weight, labile organic materials (e.g., acetate) by AOM (Yang et al, 2020). This inference was demonstrated by the identification of a complete archaeal acetogenesis pathway in the ANME-2a genome and the activity of the key enzymes in acetate generation (Yang et al, 2020). Notably, the acetate may account for a small fraction of the methane-derived labile DOC pool, which can subsequently sustain the highly divergent heterotrophic communities in the seep sediments (Valentine et al, 2005).…”