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Comparative Study
, 80 (7), 2261-9

The Cockroach Origin of the Termite Gut Microbiota: Patterns in Bacterial Community Structure Reflect Major Evolutionary Events

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Comparative Study

The Cockroach Origin of the Termite Gut Microbiota: Patterns in Bacterial Community Structure Reflect Major Evolutionary Events

Carsten Dietrich et al. Appl Environ Microbiol.

Abstract

Termites digest wood and other lignocellulosic substrates with the help of their intestinal microbiota. While the functions of the symbionts in the digestive process are slowly emerging, the origin of the bacteria colonizing the hindgut bioreactor is entirely unknown. Recently, our group discovered numerous representatives of bacterial lineages specific to termite guts in a closely related omnivorous cockroach, but it remains unclear whether they derive from the microbiota of a common ancestor or were independently selected by the gut environment. Here, we studied the bacterial gut microbiota in 34 species of termites and cockroaches using pyrotag analysis of the 16S rRNA genes. Although the community structures differed greatly between the major host groups, with dramatic changes in the relative abundances of particular bacterial taxa, we found that the majority of sequence reads belonged to bacterial lineages that were shared among most host species. When mapped onto the host tree, the changes in community structure coincided with major events in termite evolution, such as acquisition and loss of cellulolytic protists and the ensuing dietary diversification. UniFrac analysis of the core microbiota of termites and cockroaches and construction of phylogenetic tree of individual genus level lineages revealed a general host signal, whereas the branching order often did not match the detailed phylogeny of the host. It remains unclear whether the lineages in question have been associated with the ancestral cockroach since the early Cretaceous (cospeciation) or are diet-specific lineages that were independently acquired from the environment (host selection).

Figures

FIG 1
FIG 1
Relative abundances of the most prevalent bacterial phyla in the gut microbiota of different host groups. O, other insects; C, cockroaches; L, lower termites; M, T, and N, the higher termites Macrotermitinae, Termitinae, and Nasutitermitinae, respectively. Cryptocercidae and Apicotermitinae were not included because each group was represented by only a single species. The bars and horizontal lines show the ranges and median numbers of sequence reads assigned to the respective phyla. Detailed results for all bacterial phyla and individual host species are shown in Fig. S1 in the supplemental material.
FIG 2
FIG 2
Phylogenetic patterns in the community structures of the bacterial gut microbiota of the different host species. Community similarities (Bray-Curtis) were calculated based on the distributions of genus level taxa (see Table S1 in the supplemental material) and visualized by NMDS (stress, 11.3%). The symbols indicate feeding habits: generalists (□), wood feeding (▲), grass feeding (△), soil/humus feeding (○), and fungus cultivating (■). Two species of crickets (Gryllidae) and a beetle larva (Scarabaeidae) were included as outgroups. The species identifier for each data point is included in Fig. S2a in the supplemental material. The clusters were supported by both ADONIS and MRPP analyses (P < 0.001).
FIG 3
FIG 3
Relative abundances of selected bacterial lineages in the gut microbiota that contribute strongly to the separation of cockroaches, lower termites, and higher termites in the ordination analyses. The lineages were selected from the top 50 taxa (see Table S3 in the supplemental material) and subjectively sorted according to patterns (A to E) as explained in the text. The color scale is logarithmic to emphasize rare taxa. The numbers indicate host species (see Table 1). The symbols indicate feeding habits (see the legend to Fig. 2). The tree (F) illustrates a simplified phylogeny of major host lineages (a, other cockroaches; b, Blattidae; c, Cryptocercidae; d, Mastotermitidae; e, Termopsidae; f, Hodotermitidae; g, Kalotermitidae; h, Rhinotermitidae; i, Macrotermitinae; j, Apicotermitinae; k, Termitinae; l, Nasutitermitinae). The branches connecting species that harbor gut flagellates are in red.
FIG 4
FIG 4
Ternary plot of the distribution of genus level taxa across the major host groups. The area of each circle represents the relative abundance of the reads in the entire data set, the position specifies their average abundance in the respective host groups, and the colors indicate the number of host groups in which core status is attained (presence in >70% of the hosts) (the data are from Table S3 in the supplemental material). An interactive version that allows identification of the genus behind each data point of the figure is included as a supplemental file (see Fig. S3 at http://www.termites.de/brune/publ/suppl/AEM04206-13_Figure_S3.html).
FIG 5
FIG 5
Representation of core taxa in the data set based on the number of genera or sequence reads in the entire data set. Core status was assigned if a taxon was represented by >70% of the host species in a major host group (cockroaches, lower termites, and higher termites).
FIG 6
FIG 6
Cladogram of community similarities based on the core taxa common to all major host groups (unweighted UniFrac analysis of the sequences belonging to the core genera). For the sample numbers, see Table 1. The symbols indicate lifestyle: generalists (□), wood feeding (▲), grass feeding (△), soil/humus feeding (○), and fungus cultivating (■). The branches connecting species that harbor gut flagellates are in red.

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