Comparative metagenomic and metatranscriptomic analysis of hindgut paunch microbiota in wood- and dung-feeding higher termites

Abstract

Termites effectively feed on many types of lignocellulose assisted by their gut microbial symbionts. To better understand the microbial decomposition of biomass with varied chemical profiles, it is important to determine whether termites harbor different microbial symbionts with specialized functionalities geared toward different feeding regimens. In this study, we compared the microbiota in the hindgut paunch of Amitermes wheeleri collected from cow dung and Nasutitermes corniger feeding on sound wood by 16S rRNA pyrotag, comparative metagenomic and metatranscriptomic analyses. We found that Firmicutes and Spirochaetes were the most abundant phyla in A. wheeleri, in contrast to N. corniger where Spirochaetes and Fibrobacteres dominated. Despite this community divergence, a convergence was observed for functions essential to termite biology including hydrolytic enzymes, homoacetogenesis and cell motility and chemotaxis. Overrepresented functions in A. wheeleri relative to N. corniger microbiota included hemicellulose breakdown and fixed-nitrogen utilization. By contrast, glycoside hydrolases attacking celluloses and nitrogen fixation genes were overrepresented in N. corniger microbiota. These observations are consistent with dietary differences in carbohydrate composition and nutrient contents, but may also reflect the phylogenetic difference between the hosts.

Figure 1. Phylogenetic affiliation, relative abundance and habitat distribution of OTUs that are >0.5% of total bacterial community.

The bubble size represents the relative abundance of each OTU, and bubble color indicates the types of habitats where their closest relatives in the greengenes database were found. OTUs marked red were exclusively found in higher termites, orange OTUs were restricted to termites, including both higher and lower termites, green OTUs were also found in the guts and feces of other animals (e.g. cow, goat and elephant). Blue OTUs were found in other anoxic environments, such as anaerobic digesters.

Figure 2. Key metabolic differences between cow dung- and wood-feeding termites based on gene and transcript abundance profiles.

In this schematic summary, intracellular and extracellular reactions are separated by a cell membrane, but these reactions do not necessarily all occur in one cell. Green or red thin lines (including rectangle outlines) indicate genes more abundant in the A. wheeleri or N. corniger metagenome, respectively. Green or red thick lines (including rectangle highlights) indicate transcripts more abundant in the A. wheeleri or N. corniger metatranscriptome, respectively. Black lines indicate equal representation in both termite genera.

Figure 3. Taxonomic assignment of nickel-iron (NiFe) hydrogenases (a), the large subunit of iron-only (FeFe) hydrogenases (b), formyl tetrahydrofolate synthase (FTHFS) (c), and glycoside hydrolases family 3 (GH3) (d) by MEGAN using Blastp results against the NR database.