Evidence of cospeciation between termites and their gut bacteria on a geological time scale

Abstract

Termites host diverse communities of gut microbes, including many bacterial lineages only found in this habitat. The bacteria endemic to termite guts are transmitted via two routes: a vertical route from parent colonies to daughter colonies and a horizontal route between colonies sometimes belonging to different termite species. The relative importance of both transmission routes in shaping the gut microbiota of termites remains unknown. Using bacterial marker genes derived from the gut metagenomes of 197 termites and one Cryptocercus cockroach, we show that bacteria endemic to termite guts are mostly transferred vertically. We identified 18 lineages of gut bacteria showing cophylogenetic patterns with termites over tens of millions of years. Horizontal transfer rates estimated for 16 bacterial lineages were within the range of those estimated for 15 mitochondrial genes, suggesting that horizontal transfers are uncommon and vertical transfers are the dominant transmission route in these lineages. Some of these associations probably date back more than 150 million years and are an order of magnitude older than the cophylogenetic patterns between mammalian hosts and their gut bacteria. Our results suggest that termites have cospeciated with their gut bacteria since first appearing in the geological record.

Keywords: cophylogeny; endosymbionts; isoptera; metagenomics; vertical inheritance.

Figure 1.

Results of the cophylogenetic analyses performed on the marker gene COG0552 of 27 termite-specific archaeal and bacterial clades (TSCs). The cophylogenetic analyses were performed with three different methods: PACo, the generalized RF metric, and the tree alignment algorithm described by Nye et al. [66]. The transfer rates were estimated using the ML method implemented in the GeneRax software.

Figure 2.

Selected phylogenetic trees of termite-specific bacterial clades (TSCs) showing strong cophylogenetic signals with termites. The TSC phylogenetic trees were reconstructed with IQtree using the RY-recoded DNA sequence alignments from the marker gene COG0552. Phylogenetic trees of (a) the Spirochaetota Breznakiellaceae TSC26, (b) the Spirochaetota Breznakiellaceae TSC25, (c) the Fibrobacterota Fibromonas TSC11 and (d) the Desulfobacterota Adiutrix TSC10. (e) Phylogenetic tree of termites inferred from mitochondrial genomes. The diagrams below the phylogenetic trees indicate the results of the cophylogenetic analyses and the estimation of the horizontal transfer rate. Scale bars represent substitutions per site.

Figure 3.

Rate of transfer and phylogenetic trees of some termite-specific bacterial clades (TSCs) showing strong cophylogenetic signals with termites. The TSC phylogenetic trees were reconstructed with IQtree using the RY-recoded DNA sequence alignments from the marker gene COG0552. (a) Rates of horizontal transfer of 27 TSCs were estimated using the ML method implemented in the GeneRax software. Red dots represent bacterial clades showing no significant cophylogenetic signals, and cyan dots represent bacterial clades showing significant cophylogenetic signals. Tanglegrams between termites and (b) the Desulfobacterota Adiutrix TSC10 and (c) the Pseudomonadota Rhodocyclaceae TSC21. (d) Phylogenetic tree of termites inferred from mitochondrial genomes. The diagrams below the phylogenetic trees indicate the results of the cophylogenetic analyses and the estimation of the horizontal transfer rate. The scale bar represents substitutions per site.