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

作者：Tomoyuki Sato, Hirokazu Kuwahara, Kazuma Fujita, Satoko Noda, Kumiko Kihara, Akinori Yamada, Moriya Ohkuma, Yuichi Hongoh · 发表于：The ISME Journal · 年份：2013 · DOI：10.1038/ismej.2013.222 · 被引用次数：61 · 研究领域：Insect and Arachnid Ecology and Behavior、Plant and animal studies、Insect and Pesticide Research

In 1944, Harold Kirby described microorganisms living within nuclei of the protists Trichonympha in guts of termites; however, their taxonomic assignment remains to be accomplished. Here, we identified intranuclear symbionts of Trichonympha agilis in the gut of the termite Reticulitermes speratus. We isolated single nuclei of T. agilis, performed whole-genome amplification, and obtained bacterial 16S rRNA genes by PCR. Unexpectedly, however, all of the analyzed clones were from pseudogenes of 16S rRNA with large deletions and numerous sequence variations even within a single-nucleus sample. Authentic 16S rRNA gene sequences were finally recovered by digesting the nuclear DNA; these pseudogenes were present on the host Trichonympha genome. The authentic sequences represented two distinct bacterial species belonging to the phylum Verrucomicrobia, and the pseudogenes have originated from each of the two species. Fluorescence in situ hybridization confirmed that both species are specifically localized, and occasionally co-localized, within nuclei of T. agilis. Transmission electron microscopy revealed that they are distorted cocci with characteristic electron-dense and lucent regions, which resemble the intranuclear symbionts illustrated by Kirby. For these symbionts, we propose a novel genus and species, 'Candidatus Nucleococcus trichonymphae' and 'Candidatus Nucleococcus kirbyi'. These formed a termite-specific cluster with database sequences, other members of which were also d...