Extensive genomic diversity of closely related Wolbachia strains

Abstract

Using microarray-based comparative genome hybridization (mCGH), the genomic content of Wolbachia pipientis wMel from Drosophila melanogaster was compared to the closely related Wolbachia from D. innubila (wInn), D. santomea (wSan), and three strains from D. simulans (wAu, wRi, wSim). A large number of auxiliary genes are identified in these five strains, with most absent/ divergent genes being unique to a given strain. Each strain caused an average of~60 genes to be removed from the core genome. As such, these organisms do not appear to have the streamlined genomes expected of obligate intracellular bacteria. Prophage, hypothetical and ankyrin repeat genes are over-represented in the absent/divergent genes, with 21-87 % of absent/divergent genes coming from prophage regions. The only wMel region absent/divergent in all five query strains is that containing WD_0509 to WD_0511, including a DNA mismatch repair protein MutL-2, a degenerate RNase, and a conserved hypothetical protein. A region flanked by the two portions of the WO-B prophage in wMel is found in four of the five Wolbachia strains as well as on a plasmid of a rickettsial endosymbiont of Ixodes scapularis, suggesting lateral gene transfer between these two obligate intracellular species. Overall, these insect-associated Wolbachia have highly mosaic genomes, with lateral gene transfer playing an important role in their diversity and evolution. INTRODUCTIONWolbachia bacteria are common obligate intracellular endosymbionts that infect a wide variety of invertebrates, including arthropods and filarial nematodes. The arthropod-infecting Wolbachia strains are maternally inherited and exert unusual effects on host reproduction, including: (1) parthenogenesis, whereby infected virgin females produce infected female offspring, (2) male killing, whereby infected male embryos fail to develop, (3) feminization, whereby genetic males develop into reproductively capable females, and (4) cytoplasmic incompatibility, the most common phenotype, whereby the offspring of uninfected females and infected males fail to develop (Stouthamer et al., 1999;Werren et al., 2008). These phenotypes increase the number of infected hosts within a population, promoting the frequency of Wolbachia. Although insect-associated Wolbachia are typically considered reproductive parasites, some Abbreviation: mCGH, microarray comparative genome hybridization.3These authors contributed equally to this paper. et al., 2008). In addition to the above nomenclature, another convention has been proposed that combines all genes found in .1 % of strains into a species genome, and any genes in ,1 % of strains are considered of foreign origin or on the decline (Boucher et al., 2001;Lan & Reeves, 2000).In order to examine the core genome and the genetic flux between W. pipientis strains, we examined the genomic content of five strains using microarray-based comparative genomic hybridization (mCGH) on a Wolbachia microarray. DNAs from reference and query organisms are differentially labelled and competitive...

Lateral transfers of insertion sequences between Wolbachia, Cardinium and Rickettsia bacterial endosymbionts

“…The frequent ISRpe1 lateral transfers pose, however, the question of the underlying transmission mechanisms: because IS lack the machinery for lateral transfer, endoymbionts should exchange more genetic material than ISRpe1. Precisely, this pattern has occasionally been reported from recent genomic studies (Ishmael et al, 2009;Penz et al, 2012;Duplouy et al, 2013). What is yet to be established is the extent of these DNA exchanges, especially across large phylogenetic distances, and whether this leads to important innovations in endosymbionts.…”

“…In some cases, ISRpe1 transfers might be thus facilitated by the presence of WO bacteriophages that commonly jump between Wolbachia strains (Bordenstein and Wernegreen, 2004;Chafee et al, 2010;Atyame et al, 2011). Occasionally, WO bacteriophages may also undergo distant lateral transfer, as recently reported in Rickettsia (Ishmael et al, 2009), and then introduce ISRpe1 to recipient endosymbionts phylogenetically distant from donor strain. In addition, the presence of plasmids in many Cardinium and Rickettsia strains (Ogata et al, 2005;Penz et al, 2012) might serve as shuttles for transferring ISRpe1 among strains.…”

Biological Diversity of Prokaryotic Type IV Secretion Systems

“…In this context, it is intriguing that these pathogens often possess T4SS gene clusters bearing duplications of certain virB-like genes. Homologs of most of the VirB/ VirD4 genes were identified in all species of the Anaplasmataceae (Ehrlichia chaffeensis, Ehrlichia ruminantium, Anaplasma phagocytophilum, Anaplasma marginale, Wolbachia spp., Neorickettsia sennetsu) as well as the Rickettsiaceae (Rickettsia typhi, Rickettsia prowazekii, and Rickettsia conorii) (7,61,106,108,136,140,188,205,206).…”

Evolutionary aspects of toxin-producing bacteria

“…Bacteriophages and other mobile genetic elements also play important evolutionary roles in bacterial endosymbiont systems of insect hosts [279][280][281][282]. The extensive genome diversity found among parasitic arthropod bacterial symbionts (Wolbachia, Rickettsia) was shown to reside primarily in regions originating from HGT between Wolbachia strains that coinfect a diverse set of insect host cells [280,282,283].…”