Hyperthermophilic methanogenic archaea act as high-pressure CH₄ cell factories

Bioprocesses converting carbon dioxide with molecular hydrogen to methane (CH₄) are currently being developed to enable a transition to a renewable energy production system. In this study, we present a comprehensive physiological and biotechnological examination of 80 methanogenic archaea (methanogens) quantifying growth and CH₄ production kinetics at hyperbaric pressures up to 50 bar with regard to media, macro-, and micro-nutrient supply, specific genomic features, and cell envelope architecture. Our analysis aimed to systematically prioritize high-pressure and high-performance methanogens. We found that the hyperthermophilic methanococci Methanotorris igneus and Methanocaldococcoccus jannaschii are high-pressure CH₄ cell factories. Furthermore, our analysis revealed that high-performance methanogens are covered with an S-layer, and that they harbour the amino acid motif Tyr^α444 Gly^α445 Tyr^α446 in the alpha subunit of the methyl-coenzyme M reductase. Thus, high-pressure biological CH₄ production in pure culture could provide a purposeful route for the transition to a carbon-neutral bioenergy sector.