The trace amounts (0.53 ppmv) of atmospheric hydrogen gas (H) can be utilized by microorganisms to persist during dormancy. This process is catalyzed by certain Actinobacteria, Acidobacteria, and Chloroflexi, and is estimated to convert 75 × 10 g H annually, which is half of the total atmospheric H. This rapid atmospheric H turnover is hypothesized to be catalyzed by high-affinity [NiFe] hydrogenases. However, apparent high-affinity H oxidation has only been shown in whole cells, rather than for the purified enzyme. Here, we show that the membrane-associated hydrogenase from the thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV possesses a high apparent affinity (K = 140 nM) for H and that methanotrophs can oxidize subatmospheric H. Our findings add to the evidence that the group 1h [NiFe] hydrogenase is accountable for atmospheric H oxidation and that it therefore could be a strong controlling factor in the global H cycle. We show that the isolated enzyme possesses a lower affinity (K = 300 nM) for H than the membrane-associated enzyme. Hence, the membrane association seems essential for a high affinity for H. The enzyme is extremely thermostable and remains folded up to 95 °C. Strain SolV is the only known organism in which the group 1h [NiFe] hydrogenase is responsible for rapid growth on H as sole energy source as well as oxidation of subatmospheric H. The ability to conserve energy from H could increase fitness of verrucomicrobial methanotrophs in geothermal ecosystems with varying CH fluxes. We propose that H oxidation can enhance growth of methanotrophs in aerated methane-driven ecosystems. Group 1h [NiFe] hydrogenases could therefore contribute to mitigation of global warming, since CH is an important and extremely potent greenhouse gas.