Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites

Abstract

Background: Termites are among the most successful insect lineages on the globe and are responsible for providing numerous ecosystem services. They mainly feed on wood and other plant material at different stages of humification. Lignocellulose is often a principal component of such plant diet and termites largely rely on their symbiotic microbiota and associated enzymes to decompose their food efficiently. While lower termites and their gut flagellates were given larger scientific attention in the past, the gut lignocellulolytic bacteria of higher termites remain less explored. Therefore, in this study, we investigated the structure and function of gut prokaryotic microbiomes from 11 higher termite genera representative of Syntermitinae, Apicotermitinae, Termitidae and Nasutitermitinae subfamilies, broadly grouped into plant fibre- and soil-feeding termite categories. Results: Despite the different compositional structures of the studied termite gut microbiomes, reflecting well the diet and host lineage, we observed a surprisingly high functional congruency between gut metatranscriptomes from both feeding groups. The abundance of transcripts encoding for carbohydrate active enzymes as well as expression and diversity profiles of assigned glycoside hydrolase families were also similar between plant fibre- and soil-feeding termites. Yet, dietary imprints highlighted subtle metabolic differences specific to each feeding category. Roughly 0.18 % of de novo re-constructed gene transcripts were shared between the different termite gut microbiomes, making each termite gut a unique reservoir of genes encoding for potentially industrially applicable enzymes, e.g. relevant to biomass degradation. Taken together, we demonstrated the functional equivalence in microbial populations across different termite hosts.Conclusions: Our results provide valuable insight into the bacterial component of the termite gut system and significantly expand the inventory of termite prokaryotic genes participating in the deconstruction of plant biomass.

The functional evolution of termite gut microbiota

“…Contigs including genes with discordant taxonomic annotations potentially indicate horizontal gene transfers, as is common among bacteria (Ochman et al ., 2000), and were removed. We found that Bacteroidota were a significant source of GH2, GH9, GH10, GH20, GH28, GH29, GH30, GH31, and GH130 in FC and LT, while, as previously described (Marynowska et al ., 2020), they rarely encoded these GHs in non-Macrotermitinae Termitidae (WF and SF) (Figure 4, Table S8). In contrast, Fibrobacteres, which were very rare in LT, were a significant source of GH2, GH3, GH8, GH9, GH10, GH11, GH18, GH26, GH30, GH43, GH94, and GH130 in WF.…”

“…Therefore, the primary contributors of GHs are distinct between lower and higher termites. These results are consistent with previous reports indicating a possible involvement of the ectosymbiotic Bacteroidota of some oxymonadid flagellates in cellulose and hemicellulose hydrolysis (Yuki et al, 2015;Treitli et al, 2019) in lower termites, while Fibrobacteres, Spirochaeota, and/or Firmicutes are major agents in cellulose and hemicellulose degradation in higher termites (Warneke et al, 2007;He et al, 2013;Tokuda et al, 2018;Calusinska et al, 2020;Marynowska et al, 2020). Our comprehensive analyses strongly indicate that the loss of cellulolytic flagellates in the ancestor of higher termites was accompanied by a major reworking of the cellulolytic bacterial communities, from Bacteroidota in LT to Fibrobacterota and Spirochaeota in WF and to Firmicutes in SF.…”

“…Notably, the gut metagenomes of SF possessed on average fewer CAZymes, nitrogenases, reductive acetogenesis, and sulfate-reducing genes than the gut metagenomes of other termite groups. Therefore, as pointed out by Marynowska et al (2020), the gut prokaryote communities of SF retain important carbohydrate metabolism capabilities. Nevertheless, our dataset clearly indicate that these abilities are much reduced in soilfeeders compared to wood-feeders.…”

“…While metagenomics and metatranscriptomics surveys of termite guts have been carried out for an increasingly large number of termite species (Warnecke et al, 2007;He et al, 2013;Liu et al, 2018;Tokuda et al, 2018;Marynowska et al, 2020), often with the prospect of harvesting cellulolytic enzymes able to convert plant biomass into biofuel (e.g. Tartar et al, 2009;Calusinska et al, 2020), there has been a marked sampling bias towards easy-to-sample wood-feeding termite species, and species with pest status.…”

“…Investigations of termite gut microbe genomes has revealed that, in addition to the production of enzymes involved in lignocellulose digestion, gut microbes have numerous nutritional functions, including nitrogen fixation and recycling abilities that supplement the nitrogen-poor diet of their host (Lilburn et al ., 2001; Yamada et al ., 2007; Hongoh et al ., 2008; Ohkuma, M. & Brune, 2011). While metagenomics and metatranscriptomics surveys of termite guts have been carried out for an increasingly large number of termite species (Warnecke et al ., 2007; He et al ., 2013; Liu et al ., 2018; Tokuda et al ., 2018; Marynowska et al ., 2020), often with the prospect of harvesting cellulolytic enzymes able to convert plant biomass into biofuel ( e.g. Tartar et al ., 2009; Calusinska et al ., 2020), there has been a marked sampling bias towards easy-to-sample wood-feeding termite species, and species with pest status.…”