Diversification of methanogens into hyperalkaline serpentinizing environments through adaptations to minimize oxidant limitation

Elizabeth M Fones,Eric S Boyd,Daniel R Colman,Emily A Kraus,John R Spear,Alexis S Templeton,Ramunas Stepanauskas

doi:10.1038/s41396-020-00838-1

Abstract

Metagenome assembled genomes (MAGs) and single amplified genomes (SAGs) affiliated with two distinct Methanobacterium lineages were recovered from subsurface fracture waters of the Samail Ophiolite, Sultanate of Oman. Lineage Type I was abundant in waters with circumneutral pH, whereas lineage Type II was abundant in hydrogen rich, hyperalkaline waters. Type I encoded proteins to couple hydrogen oxidation to CO2 reduction, typical of hydrogenotrophic methanogens. Surprisingly, Type II, which branched from the Type I lineage, lacked homologs of two key oxidative [NiFe]-hydrogenases. These functions were presumably replaced by formate dehydrogenases that oxidize formate to yield reductant and cytoplasmic CO2 via a pathway that was unique among characterized Methanobacteria, allowing cells to overcome CO2/oxidant limitation in high pH waters. This prediction was supported by microcosm-based radiotracer experiments that showed significant biological methane generation from formate, but not bicarbonate, in waters where the Type II lineage was detected in highest relative abundance. Phylogenetic analyses and variability in gene content suggested that recent and ongoing diversification of the Type II lineage was enabled by gene transfer, loss, and transposition. These data indicate that selection imposed by CO2/oxidant availability drove recent methanogen diversification into hyperalkaline waters that are heavily impacted by serpentinization.

Highlights

Hydrogen (H2) links the geosphere to the biosphere and has likely done so since early in Earth’s history [1,2,3,4]
Two phylogenetically distinct lineages affiliated with Methanobacterium were the sole methanogens recovered from subsurface well waters from the Samail Ophiolite (Fig. 1)
One Metagenome assembled genomes (MAGs) (Type I) represented an abundant microbial lineage in a well with circumneutral water (WAB188: pH 7.6), whereas another MAG (Type II) represented a lineage that was abundant in a well with hyperalkaline water, including samples collected at both 50 m (NSHQ14B: pH 11.1) and 85 m depths (NSHQ14C: pH 11.3) (Fig. 1A)

Summary

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Hydrogen (H2) links the geosphere to the biosphere and has likely done so since early in Earth’s history [1,2,3,4]. CH4 in hyperalkaline, highly serpentinized waters typically exhibits isotopically heavy carbon (δ13C-CH4>−40‰) [13, 25, 30, 31], a finding that has been suggested to result from abiotic processes or biological methanogenesis under extreme DIC limitation [25, 32, 33] Support for the latter interpretation includes experimental evidence demonstrating that biological methanogenesis under carbon-limited conditions can result in relatively high δ13C-CH4 values [34] and the presence of lipid biomarkers associated with methanogenic archaea recovered from globally distributed serpentinizing environments that exhibit high 13C values [35, 36]. Phylogenomic and SCG approaches are used to describe the diversification of methanogens in hyperalkaline waters resulting from serpentinization and to identify the mechanisms involved in their apparent speciation

Materials and methods

Results and discussion

Compliance with ethical standards