Intra- and Interspecific Comparisons of Bacterial Diversity and Community Structure Support Coevolution of Gut Microbiota and Termite Host

Abstract

We investigated the bacterial gut microbiota from 32 colonies of wood-feeding termites, comprising four Microcerotermes species (Termitidae) and four Reticulitermes species (Rhinotermitidae), using terminal restriction fragment length polymorphism analysis and clonal analysis of 16S rRNA. The obtained molecular community profiles were compared statistically between individuals, colonies, locations, and species of termites. Both analyses revealed that the bacterial community structure was remarkably similar within each termite genus, with small but significant differences between sampling sites and/or termite species. In contrast, considerable differences were found between the two termite genera. Only one bacterial phylotype (defined with 97% sequence identity) was shared between the two termite genera, while 18% and 50% of the phylotypes were shared between two congeneric species in the genera Microcerotermes and Reticulitermes, respectively. Nevertheless, a phylogenetic analysis of 228 phylotypes from Microcerotermes spp. and 367 phylotypes from Reticulitermes spp. with other termite gut clones available in public databases demonstrated the monophyly of many phylotypes from distantly related termites. The monophyletic "termite clusters" comprised of phylotypes from more than one termite species were distributed among 15 bacterial phyla, including the novel candidate phyla TG2 and TG3. These termite clusters accounted for 95% of the 960 clones analyzed in this study. Moreover, the clusters in 12 phyla comprised phylotypes from more than one termite (sub)family, accounting for 75% of the analyzed clones. Our results suggest that the majority of gut bacteria are not allochthonous but are specific symbionts that have coevolved with termites and that their community structure is basically consistent within a genus of termites.Termites harbor an abundance and diversity of gut bacteria, which are thought to play essential roles in the carbon and nitrogen metabolism of their host termites. While these characteristics of gut bacteria have been extensively studied by tracing the flow of carbon and nitrogen or characterizing isolated strains of bacteria (5, 25), the bacterial microbiota has remained a black box due to difficulties in cultivation of most of these bacteria. This has been an obstacle to a comprehensive understanding of symbiosis between gut bacteria and their host termites. Recently, we conducted a detailed census of the bacterial community in the gut of the termite Reticulitermes speratus by analyzing clones of 16S rRNA (18,19). We found 314 phylotypes (defined with 97.0% sequence identity) of 16S rRNA from 1,923 analyzed clones. The majority of the clones were affiliated with groups of anaerobic bacteria such as the genus Treponema and the orders Clostridiales and Bacteroidales, and most of the phylotypes were found for the first time. Many of them constituted novel lineages in several bacterial phyla, including the candidate phylum termite group I (TG1), which was one of the dominant groups in R. speratu...

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