Termite mounds contain distinct methanotroph communities that are kinetically adapted to elevated methane concentrations

Abstract

Termite mounds have recently been confirmed to mitigate approximately half of termite methane (CH4) emissions, but the aerobic methane-oxidizing bacteria (methanotrophs) responsible for this consumption have not been resolved. Here we describe the abundance, composition, and kinetics of the methanotroph communities in the mounds of three distinct termite species. We show that methanotrophs are rare members of the termite mound biosphere and have a comparable abundance, but distinct composition, to those of adjoining soil samples. Across all mounds, the most abundant and prevalent particulate methane monooxygenase sequences detected were affiliated with Upland Soil Cluster (USC), with sequences homologous to Methylocystis and Tropical Upland Soil Cluster also detected. The Michaelis-Menten kinetics of CH4 oxidation in mounds were estimated from in situ reaction rates. The apparent CH4 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 CH4 source such as landfill-cover soils. The rate constant of CH4 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 CH4 emissions have selected for unique methanotroph communities that are kinetically adapted to elevated CH4 concentrations. However, factors other than substrate concentration appear to limit methanotroph abundance and hence these bacteria only partially mitigate termite-derived CH4 emissions. Our results also highlight the predominant role of USC in an environment with elevated CH4 concentrations and suggest a higher functional diversity within this group than previously recognised.