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 Methylacidiphilum can grow autotrophically on hydrogen gas (H2), but it is unknown whether this also holds for their mesophilic counterparts from the genus Methylacidimicrobium. To determine this, we examined H2 consumption and CO2 fixation by the mesophilic verrucomicrobial methanotroph Methylacidimicrobium tartarophylax 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.
Highlights
Atmospheric concentrations of the strong greenhouse gas methane (CH4) are increasing due to anthropogenic activities (Kirschke et al, 2013)
Cells from a continuous culture grown on methane under O2 limitation showed hydrogen respiration rates below 1 nmol O2 · min−1 · mg dry weight (DW)−1 when the oxygen concentration in the respiration chamber was above 100 μM (Table 1) and again elevated rates were measured when O2 concentrations were below 30 μM (4.1 and 2.8 nmol O2 · min−1 · mg DW−1; Table 1)
We have shown that the mesophilic Methylacidimicrobium tartarophylax strain 4AC is able to grow as an autotroph on hydrogen gas as sole energy source under oxygen-limited conditions
Summary
Atmospheric concentrations of the strong greenhouse gas methane (CH4) are increasing due to anthropogenic activities (Kirschke et al, 2013). For many years it was believed that methane oxidation was a feature restricted to the subphyla Alpha- and Gammaproteobacteria (Op den Camp et al, 2009). This view was rejected due to the description of novel aerobic methanotrophs belonging to the phylum Verrucomicrobia (Dunfield et al, 2007; Pol et al, 2007; Islam et al, 2008). Methanotrophy by thermophilic members of the Verrucomicrobia phylum is an extreme affair, since they can grow on methane below pH 1 and at temperatures up to 65◦C (Op den Camp et al, 2009)
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