Dataset Information

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

ABSTRACT: 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 detected within nuclei of various gut protists, including both parabasalids and oxymonads. We suggest that this group is widely distributed as intranuclear symbionts of diverse protists in termite guts and that they might have affected the evolution of the host genome through lateral gene transfer.

SUBMITTER: Sato T

PROVIDER: S-EPMC3996698 | biostudies-literature | 2014 May

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

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

Sato Tomoyuki T Kuwahara Hirokazu H Fujita Kazuma K Noda Satoko S Kihara Kumiko K Yamada Akinori A Ohkuma Moriya M Hongoh Yuichi Y

The ISME journal 20131212 5

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 16 ...[more]

PMID: 24335826

Similar Datasets

Project description:Termites and their gut microbes engage in fascinating dietary mutualisms. Less is known about how these complex symbioses have evolved after first emerging in an insect ancestor over 120 million years ago. Here we examined a bacterial gene, formate dehydrogenase (fdhF), that is key to the mutualism in 8 species of "higher" termite (members of the Termitidae, the youngest and most biomass-abundant and species-rich termite family). Patterns of fdhF diversity in the gut communities of higher termites contrasted strongly with patterns in less-derived (more-primitive) insect relatives (wood-feeding "lower" termites and roaches). We observed phylogenetic evidence for (i) the sweeping loss of several clades of fdhF that may reflect extinctions of symbiotic protozoa and, importantly, bacteria dependent on them in the last common ancestor of all higher termites and (ii) a radiation of genes from the (possibly) single allele that survived. Sweeping gene loss also resulted in (iii) the elimination of an entire clade of genes encoding selenium (Se)-independent enzymes from higher termite gut communities, perhaps reflecting behavioral or morphological innovations in higher termites that relaxed preexisting environmental limitations of Se, a dietary trace element. Curiously, several higher termite gut communities may have subsequently reencountered Se limitation, reinventing genes for Se-independent proteins via convergent evolution. Lastly, the presence of a novel fdhF lineage within litter-feeding and subterranean higher (but not other) termites may indicate recent gene "invasion" events. These results imply that cascades of perturbation and adaptation by distinct evolutionary mechanisms have impacted the evolution of complex microbial communities in a highly successful lineage of insects. Since patterns of relatedness between termite hosts are broadly mirrored by the relatedness of their symbiotic gut microbiota, coevolution between hosts and gut symbionts is rightly considered an important force that has shaped dietary mutualism since its inception over 120 million years ago. Apart from that concerning lateral gene or symbiont transfer between termite gut communities (for which no evidence yet exists), there has been little discussion of alternative mechanisms impacting the evolution of mutualism. Here we provide strong gene-based evidence for past environmental perturbations creating significant upheavals that continue to reverberate throughout the gut communities of species comprising a single termite lineage. We suggest that symbiont extinction events, sweeping gene losses, evolutionary radiations, relaxation and reemergence of key nutritional pressures, convergent evolution of similar traits, and recent gene invasions have all shaped gene composition in the symbiotic gut microbial communities of higher termites, currently the most dominant and successful termite family on Earth.

Dataset Information

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

Publications

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

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets