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 (R2 = 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.

PhyloPlus: a Universal Tool for Phylogenetic Interrogation of Metagenomic Communities

“…Data analysis metrics which incorporate phylogeny into inferences of biological diversity exist and have been successfully employed to describe different communities ( 28 , 29 ). Yet despite the theoretical advantages posited by the incorporation of phylogeny, its use in microbial metagenomics is still limited ( 2 – 5 , 13 – 19 , 30 , 31 ). This underutilization of phylogeny arises in large part due to the difficulty of constructing a comprehensive microbial phylogeny in which all members of a diverse community are represented.…”

“…Traditionally, to compare communities groupwise, permutation is performed by randomly shuffling the labels on the rows which identify each community as belonging to a particular group ( 50 ). While this approach is widely applicable ( 13 , 14 , 17 , 32 ), shuffling grouping labels caused variation in aspects such as species richness and occupancy rates across communities. The less-constrained models, therefore, could cause potential inflation of type I errors ( 40 ).…”

“…The field of microbial community studies has exploded in part due to technical advances in high-throughput sequencing and post-sequencing bioinformatics. It has also greatly expanded because of the observed importance of microbial activities to a wide array of biological processes, including but not limited to human health (e.g., human microbiome) ( 1 – 10 ), agricultural safety and management ( 11 – 13 ), and environmental diversity and conservation ( 14 – 20 ).…”

“…Given the fact that evolutionary relationships are not equivalent or irrelevant among different species, especially when quantifying differences among highly diverse communities, metrics incorporating phylogenetic information have been proposed, such as Faith’s index and UniFrac distance ( 28 , 29 ). However, even though incorporating evolutionary information can aid in comparative community studies, phylogenetic metrics are still underutilized in this field ( 2 – 5 , 13 – 19 , 30 , 31 ). This lack of use is partially due to the difficulty of constructing a robust molecular phylogeny for the diverse set of microbes found within natural metagenomic communities.…”

Comparing the succession of microbial communities throughout development in field and laboratory nests of the ambrosia beetle Xyleborinus saxesenii

“…Beetles can counteract this effect to a limited degree by recycling their feces ( Abrahamson and Norris, 1970 ; De Fine Licht and Biedermann, 2012 ) and expansion of their tunnel systems inside the wood, but latter is strongly constrained by intraspecific competition and general degradation of the wood (which is typically colonized shortly after the death of the host tree) ( Kirkendall et al, 2015 ; Birkemoe et al, 2018 ). Second, while fungus gardens of ants and termites are very exposed to microorganisms that are constantly brought in with the new plant substrate and the surrounding soil ( Pagnocca et al, 2012 ; Estrada et al, 2014 ; Chiri et al, 2020 , 2021 ; Chen et al, 2021 ), gardens of ambrosia beetles are only exposed to microorganisms (i) already present in the wood at colonization (i.e., endosymbionts), (ii) initially brought in with the nest-founding beetle(s), or (iii) entering gardens from the surrounding wood over time. In relation, this massively reduces the exposure of ambrosia beetles to microbial threats and also explains their comparatively less advanced techniques of pathogen control ( Mighell and Van Bael, 2016 ; Diehl et al, 2022 ).…”