Widespread soil bacterium that oxidizes atmospheric methane

Abstract

The global atmospheric level of methane (CH₄), the second most important greenhouse gas, is currently increasing by ∼10 million tons per year. Microbial oxidation in unsaturated soils is the only known biological process that removes CH₄ from the atmosphere, but so far, bacteria that can grow on atmospheric CH₄ have eluded all cultivation efforts. In this study, we have isolated a pure culture of a bacterium, strain MG08 that grows on air at atmospheric concentrations of CH₄ [1.86 parts per million volume (p.p.m.v.)]. This organism, named <i>Methylocapsa gorgona</i>, is globally distributed in soils and closely related to uncultured members of the upland soil cluster α. CH₄ oxidation experiments and ¹³C-single cell isotope analyses demonstrated that it oxidizes atmospheric CH₄ aerobically and assimilates carbon from both CH₄ and CO₂ Its estimated specific affinity for CH₄ (a⁰_s) is the highest for any cultivated methanotroph. However, growth on ambient air was also confirmed for <i>Methylocapsa acidiphila</i> and <i>Methylocapsa aurea</i>, close relatives with a lower specific affinity for CH₄, suggesting that the ability to utilize atmospheric CH₄ for growth is more widespread than previously believed. The closed genome of <i>M. gorgona</i> MG08 encodes a single particulate methane monooxygenase, the serine cycle for assimilation of carbon from CH₄ and CO₂, and CO₂ fixation via the recently postulated reductive glycine pathway. It also fixes dinitrogen and expresses the genes for a high-affinity hydrogenase and carbon monoxide dehydrogenase, suggesting that atmospheric CH₄ oxidizers harvest additional energy from oxidation of the atmospheric trace gases carbon monoxide (0.2 p.p.m.v.) and hydrogen (0.5 p.p.m.v.).