PJ-166:

Evolution of verrucomicrobia from ectosymbionts to endonuclear symbionts of protists in the termite gut

Protists in the termite gut harbor symbiotic bacteria on their cell surface, within the cytoplasm, and occasionally even within the nucleoplasm (1). Harold Kirby, in 1944, described microorganisms living within nuclei of the protists Trichonympha in the termite gut, and recently, we identified them as two novel species of verrucomicrobia belonging to a novel genus, Candidatus Nucleococcus (2). In the present study, we further analysed the localization and phylogenetic positions of verrucomicrobial gut symbionts in diverse termite species based on the 16S rRNA genes.
We collected cells of each protist species with a micromanipulator in several termite species, performed whole-genome amplification (WGA), and acquired verrucomicrobial 16S rRNA genes by PCR using the WGA products as templates. Each of the obtained verrucomicrobial phylotypes was located by FISH analyses and detected from cells of specific host protist species. The results indicate that the host-symbiont relationship is basically species-specific. Furthermore, closely related protist species harbor closely related verrucomicrobial phylotypes, suggesting their cospeciation to a certain extent. Indeed, we observed that the verrucomicrobial cells were separated to each daughter nucleus of a protist cell when it divided; the verrucomicrobial endonuclear symbionts can be vertically transmitted.
Interestingly, we also found that the verrucomicrobial gut symbionts are not confined to the nucleoplasm of the protist cells, but also inhabit their paranuclear region, entire cytoplasm, cell surface, or intestinal wall of the termite. These localizations are not random but are strongly correlated with the lineages they belong to. Our study suggests that the verrucomicrobia have evolved from ectosymbionts to cytoplasmic symbionts, and finally to the endonuclear symbionts.

(1) Hongho Y., Jpn. J. Protozool.44: 115-129 (2011)
(2) Sato T., Kuwahara H., et al., ISME J. 8: 1008-1019 (2014)

keywords:verrucomicrobia ,Evolution ,ectosymbionts ,cytoplasmic symbionts,endonuclear symbionts