Strict cospeciation of devescovinid flagellates and Bacteroidales ectosymbionts in the gut of dry‐wood termites (Kalotermitidae)

Abstract

SummaryThe surface of many termite gut flagellates is colonized with a dense layer of bacteria, yet little is known about the evolutionary relationships of such ectosymbionts and their hosts. Here we investigated the molecular phylogenies of devescovinid flagellates (Devescovina spp.) and their symbionts from a wide range of dry-wood termites (Kalotermitidae). From species-pure flagellate suspensions isolated with micropipettes, we obtained SSU rRNA gene sequences of symbionts and host. Phylogenetic analysis showed that the Devescovina spp. present in many species of Kalotermitidae form a monophyletic group, which includes also the unique devescovinid flagellate Caduceia versatilis. All members of this group were consistently associated with a distinct lineage of Bacteroidales, whose location on the cell surface was confirmed by fluorescence in situ hybridization. The well-supported congruence of the phylogenies of devescovinids and their ectosymbionts documents a strict cospeciation. In contrast, the endosymbionts of the same flagellates ('Endomicrobia') were clearly polyphyletic and must have been acquired independently by horizontal transfer from other flagellate lineages. Also the Bacteroidales ectosymbionts of Oxymonas flagellates present in several Kalotermitidae belonged to several distantly related lines of descent, underscoring the general perception that the evolutionary history of flagellate-bacteria symbioses in the termite gut is complex.

Bacteroidales ectosymbionts of gut flagellates shape the nitrogen-fixing community in dry-wood termites

“…nifH homologs in capillary-picked flagellates Cloning and sequence analysis of the eukaryotic SSU rRNA genes in the capillary-picked suspensions of D. arta and S. tabogae confirmed the purity of the preparations. The sequence of D. arta was identical to that obtained in a previous study of the same termite (FN377761; Desai et al, 2010); the newly obtained SSU rRNA gene sequence of S. tabogae has been submitted to GenBank (FN649413).…”

“…There is abundant evidence that the bacterial symbionts of most gut flagellates are specific for and even co-speciate with their respective hosts (for example, Stingl et al, 2005;Noda et al, 2006Noda et al, , 2007Noda et al, , 2009Ikeda-Ohtsubo et al, 2007;Ohkuma et al, 2007;Ikeda-Ohtsubo and Brune, 2009;Desai et al, 2010;Strassert et al, 2010). The nitrogenfixing nature of the bacterial symbionts has been documented for at least two of these symbiotic pairs (Hongoh et al, 2008b and this study) and may indeed be the evolutionary driver for many of these associations.…”

“…devescovinae', the ectosymbiont of the most abundant gut flagellates of many dry-wood termites (Devescovina spp. ; Desai et al, 2010). Also the nifH expression patterns in other dry-wood termites appear to be shaped by flagellate symbionts.…”

“…As specific associations between gut flagellates and symbiotic Bacteroidales are common also in dry-wood termites (Noda et al, 2006;Desai et al, 2010;Strassert et al, 2010), it seemed possible that the high activities of nitrogen fixation present in this termite family are due to the symbiont of their flagellates. Here, we identified the active diazotrophs in representatives of four major genera of Kalotermitidae (Neotermes castaneus, Cryptotermes longicollis, Kalotermes flavicollis and Incisitermes marginipennis).…”

Intranuclear verrucomicrobial symbionts and evidence of lateral gene transfer to the host protist in the termite gut

“…Other members of the termite-specific cluster in Figure 2 included uncultured phylotypes recovered from the cells of the protist Oxymonas sp. in the gut of Cryptotermes secundus (Desai et al, 2010). In the present study, we identified members of this cluster as intranuclear symbionts of both oxymonad and parabasalid protists ( Figure 5).…”