The Acidophilic Methanotroph Methylacidimicrobium tartarophylax 4AC Grows as Autotroph on H2 Under Microoxic Conditions

Abstract

Emissions of the strong greenhouse gas methane (CH₄) to the atmosphere are mitigated by methanotrophic microorganisms. Methanotrophs found in extremely acidic geothermal systems belong to the phylum Verrucomicrobia. Thermophilic verrucomicrobial methanotrophs from the genus <i>Methylacidiphilum</i> can grow autotrophically on hydrogen gas (H₂), but it is unknown whether this also holds for their mesophilic counterparts from the genus <i>Methylacidimicrobium</i>. To determine this, we examined H₂ consumption and CO₂ fixation by the mesophilic verrucomicrobial methanotroph <i>Methylacidimicrobium tartarophylax</i> 4AC. We found that strain 4AC grows autotrophically on H₂ with a maximum growth rate of 0.0048 h^-1 and a yield of 2.1 g dry weight⋅mol H₂ ^-1, which is about 12 and 41% compared to the growth rate and yield on methane, respectively. The genome of strain 4AC only encodes for an oxygen-sensitive group 1b [NiFe] hydrogenase and H₂ is respired only when oxygen concentrations are below 40 μM. Phylogenetic analysis and genomic comparison of methanotrophs revealed diverse [NiFe] hydrogenases, presumably with varying oxygen sensitivity and affinity for H₂, which could drive niche differentiation. Our results show that both thermophilic and mesophilic verrucomicrobial methanotrophs can grow as autotrophs on H₂ as a sole energy source. Our results suggest that verrucomicrobial methanotrophs are particularly well-equipped to thrive in hostile volcanic ecosystems, since they can consume H₂ as additional energy source.