Termite mounds contain soil-derived methanotroph communities kinetically adapted to elevated methane concentrations

Termite mounds have recently been confirmed to mitigate approximately half of termite methane (CH(4)) emissions, but the aerobic CH(4) oxidising bacteria (methanotrophs) responsible for this consumption have not been resolved. Here, we describe the abundance, composition and CH(4) oxidation kinetics of the methanotroph communities in the mounds of three distinct termite species sampled from Northern Australia. Results from three independent methods employed show that methanotrophs are rare members of microbial communities in termite mounds, with a comparable abundance but distinct composition to those of adjoining soil samples. Across all mounds, the most abundant and prevalent methane monooxygenase sequences were affiliated with upland soil cluster α (USCα), with sequences homologous to Methylocystis and tropical upland soil cluster (TUSC) also detected. The reconstruction of a metagenome-assembled genome of a mound USCα representative highlighted the metabolic capabilities of this group of methanotrophs. The apparent Michaelis–Menten kinetics of CH(4) oxidation in mounds were estimated from in situ reaction rates. Methane affinities of the communities were in the low micromolar range, which is one to two orders of magnitude higher than those of upland soils, but significantly lower than those measured in soils with a large CH(4) source such as landfill cover soils. The rate constant of CH(4) oxidation, as well as the porosity of the mound material, were significantly positively correlated with the abundance of methanotroph communities of termite mounds. We conclude that termite-derived CH(4) emissions have selected for distinct methanotroph communities that are kinetically adapted to elevated CH(4) concentrations. However, factors other than substrate concentration appear to limit methanotroph abundance and hence these bacteria only partially mitigate termite-derived CH(4) emissions. Our results also highlight the predominant role of USCα in an environment with elevated CH(4) concentrations and suggest a higher functional diversity within this group than previously recognised.