Wolbachiagenome integrated in an insect chromosome: Evolution and fate of laterally transferred endosymbiont genes

Abstract

Recent accumulation of microbial genome data has demonstrated that lateral gene transfers constitute an important and universal evolutionary process in prokaryotes, while those in multicellular eukaryotes are still regarded as unusual, except for endosymbiotic gene transfers from mitochondria and plastids. Here we thoroughly investigated the bacterial genes derived from a Wolbachia endosymbiont on the nuclear genome of the beetle Callosobruchus chinensis. Exhaustive PCR detection and Southern blot analysis suggested that ∼30% of Wolbachia genes, in terms of the gene repertoire of wMel, are present on the insect nuclear genome. Fluorescent in situ hybridization located the transferred genes on the proximal region of the basal short arm of the X chromosome. Molecular evolutionary and other lines of evidence indicated that the transferred genes are probably derived from a single lateral transfer event. The transferred genes were, for the length examined, structurally disrupted, freed from functional constraints, and transcriptionally inactive. Hence, most, if not all, of the transferred genes have been pseudogenized. Notwithstanding this, the transferred genes were ubiquitously detected from Japanese and Taiwanese populations of C. chinensis, while the number of the transferred genes detected differed between the populations. The transferred genes were not detected from congenic beetle species, indicating that the transfer event occurred after speciation of C. chinensis, which was estimated to be one or several million years ago. These features of the laterally transferred endosymbiont genes are compared with the evolutionary patterns of mitochondrial and plastid genome fragments acquired by nuclear genomes through recent endosymbiotic gene transfers.

Horizontal gene transfer in the acquisition of novel traits by metazoans

“…30% with respect to the gene repertoire) have been found in the genome of the bean beetle Callosobruchus chinensis. However, although a low transcriptional level could be detected, most of the genes in these transferred fragments have been pseudogenized [49,50].…”

Longicorn beetle that vectors pinewood nematode carries manyWolbachiagenes on an autosome

“…(g) Phylogenetic affinity to laterally transferred Wolbachia genes in C. chinensis Of the 31 Wolbachia genes detected from M. alternatus, 11 genes ( fabF, gltP, mpp2, ftsH, gyrA, qor, ftsZ, hslU, thy1, priN and petA) were also found in laterally transferred Wolbachia genes from the adzuki bean beetle C. chinensis (Nikoh et al 2008). Molecular phylogenetic analyses revealed that, as with the ftsZ gene alone (figure 1), the Wolbachia genes from M. alternatus consistently exhibited phylogenetic affinity to the laterally transferred Wolbachia genes in C. chinensis (figure S2 in the supplementary electronic material).…”

“…The constant and intimate contact between the eukaryotic host cells and inhabiting bacterial associates may predispose the exchange of genetic materials between the partners. Among insects and nematodes, Wolbachia endosymbionts have been identified as a major source of laterally transferred genes in their genomes (Kondo et al 2002b;Fenn et al 2006;Dunning Hotopp et al 2007;Nikoh et al 2008;Klasson et al 2009;Nikoh & Nakabachi 2009;Woolfit et al 2009). …”

Abbreviations and acronyms

“…LGT of fragments of the Wolbachia genome (total size approximately 1.2 Mb), ranging from 500 base pairs to more than 1 Mb, have been observed in many invertebrates, including beetles (Nikoh et al, 2008), grasshoppers (Funkhouser-Jones, 2015;Toribio-Fernández et al, 2017), wasps (Dunning-Hotopp et al, 2007), fruit flies (Dunning-Hotopp et al, 2007;Klasson et al, 2014;Choi, Bubnell and Aquadro, 2015;Morrow et al, 2015), tsetse flies (Brelsfoard et al, 2014;Nakao et al, 2016), butterflies and moths , kissing bugs (Mesquita et al, 2015), mosquitoes (Klasson et al, 2009;Hou et al, 2014), filarial nematodes (Fenn et al, 2006;Dunning-Hotopp et al, 2007;Keroack et al, 2016) and spiders (Baldo et al, 2008).…”