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, 276 (1655), 239-45

Inheritance and Diversification of Symbiotic Trichonymphid Flagellates From a Common Ancestor of Termites and the Cockroach Cryptocercus

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Inheritance and Diversification of Symbiotic Trichonymphid Flagellates From a Common Ancestor of Termites and the Cockroach Cryptocercus

Moriya Ohkuma et al. Proc Biol Sci.

Abstract

Cryptocercus cockroaches and lower termites harbour obligate, diverse and unique symbiotic cellulolytic flagellates in their hindgut that are considered critical in the development of social behaviour in their hosts. However, there has been controversy concerning the origin of these symbiotic flagellates. Here, molecular sequences encoding small subunit rRNA and glyceraldehyde-3-phosphate dehydrogenase were identified in the symbiotic flagellates of the order Trichonymphida (phylum Parabasalia) in the gut of Cryptocercus punctulatus and compared phylogenetically to the corresponding species in termites. In each of the monophyletic lineages that represent family-level groups in Trichonymphida, the symbionts of Cryptocercus were robustly sister to those of termites. Together with the recent evidence for the sister-group relationship of the host insects, this first comprehensive study comparing symbiont molecular phylogeny strongly suggests that a set of symbiotic flagellates representative of extant diversity was already established in an ancestor common to Cryptocercus and termites, was vertically transmitted to their offspring, and subsequently became diversified to distinct levels, depending on both the host and the symbiont lineages.

Figures

Figure 1
Figure 1
FISH identification of trichonymphid symbionts in the gut of Cryptocercus. Six rows correspond to FISH experiments against the gut content of C. punctulatus using specific probes for the trichonymphid SSU rRNA gene sequences. The target sequence is shown below images in each row. (a (i)–(vi)) Detection of sequence-specific hybridizations (in green), (b (i)–(vi)) the control detections of all the eukaryote cells (in red) and (c (i)–(vi)) the phase-contrast images of the same microscopic field. The amorphous yellow derives from autofluorescence probably from ingested wood. Arrowheads in the phase-contrast images indicate the cells that gave positive signals for sequence-specific FISH detection. The identified trichonymphid species were as follows: T. acuta for Cp20; Trichonympha sp. for Cp07; U. talea for Cp13; B. ufalula for Cp49; and Barbulanympha spp. for Cp38 and Cp26. Bars in the phase-contrast images represent 100 μm.
Figure 2
Figure 2
Unrooted ML tree inferred from nuclear SSU rRNA gene sequences of trichonymphids, using 1142 unambiguously aligned positions. The sequences in bold were obtained from trichonymphids in the gut of C. punctulatus. The name of host termite species is shown in parentheses after each flagellate taxon. The family-level groups and sequences of termite Trichonympha are indicated with vertical bars. The accession numbers of the sequences of the symbionts in termites have been reported in Ohkuma et al. (2005) and Noda et al. (2007). Bayesian posterior probability and PHYML bootstrap value (divided by slash) are indicated in each node except nodes for branches of termite Trichonympha. Asterisks at nodes indicate the full support (100/100). Scale bars indicate 0.10 substitutions per position.
Figure 3
Figure 3
ML tree of GAPDH sequences showing sister relationships of trichonymphid symbionts between Cryptocercus and termites. The tree was inferred from 324 amino acid positions aligned unambiguously. The parabasalid sequences outside Trichonymphida were used as out-groups owing to the clear dichotomy between Trichonymphida and the other parabasalids as well as the most likely root position of parabasalids at the node dividing these groups (Ohkuma et al. 2007a,b). The sequences of trichonymphids in C. punctulatus are shown in bold. The family-level groups (T: Trichonymphidae, E: Eucomonymphidae plus Teranymphidae) and the orders Spirotrichonymphida (S) and Cristamonadida (C) are indicated with vertical bars. The accession numbers of the other sequences have been reported in Gerbod et al. (2004) and Ohkuma et al. (2007a,b). Bayesian posterior probability and PHYML bootstrap value (divided by slash) are indicated in each node. Asterisks at nodes indicate full support (100/100). Scale bars indicate 0.10 substitutions per position.

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