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Termite gas emissions select for hydrogenotrophic microbial communities in termite mounds.

ABSTRACT: Organoheterotrophs are the dominant bacteria in most soils worldwide. While many of these bacteria can subsist on atmospheric hydrogen (H₂), levels of this gas are generally insufficient to sustain hydrogenotrophic growth. In contrast, bacteria residing within soil-derived termite mounds are exposed to high fluxes of H₂ due to fermentative production within termite guts. Here, we show through community, metagenomic, and biogeochemical profiling that termite emissions select for a community dominated by diverse hydrogenotrophic Actinobacteriota and Dormibacterota. Based on metagenomic short reads and derived genomes, uptake hydrogenase and chemosynthetic RuBisCO genes were significantly enriched in mounds compared to surrounding soils. In situ and ex situ measurements confirmed that high- and low-affinity H₂-oxidizing bacteria were highly active in the mounds, such that they efficiently consumed all termite-derived H₂ emissions and served as net sinks of atmospheric H₂ Concordant findings were observed across the mounds of three different Australian termite species, with termite activity strongly predicting H₂ oxidation rates (R ² = 0.82). Cell-specific power calculations confirmed the potential for hydrogenotrophic growth in the mounds with most termite activity. In contrast, while methane is produced at similar rates to H₂ by termites, mounds contained few methanotrophs and were net sources of methane. Altogether, these findings provide further evidence of a highly responsive terrestrial sink for H₂ but not methane and suggest H₂ availability shapes composition and activity of microbial communities. They also reveal a unique arthropod-bacteria interaction dependent on H₂ transfer between host-associated and free-living microbial communities.

SUBMITTER: Chiri E

PROVIDER: S-EPMC8325338 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Termite mounds have recently been confirmed to mitigate approximately half of termite methane (CH4) emissions, but the aerobic CH4 oxidising bacteria (methanotrophs) responsible for this consumption have not been resolved. Here, we describe the abundance, composition and CH4 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 CH4 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 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 distinct 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 USCα in an environment with elevated CH4 concentrations and suggest a higher functional diversity within this group than previously recognised.

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Termite gas emissions select for hydrogenotrophic microbial communities in termite mounds.

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