Draft genome sequence of the male-killing Wolbachia strain wBol1 reveals recent horizontal gene transfers from diverse sources

Abstract

BackgroundThe endosymbiont Wolbachia pipientis causes diverse and sometimes dramatic phenotypes in its invertebrate hosts. Four Wolbachia strains sequenced to date indicate that the constitution of the genome is dynamic, but these strains are quite divergent and do not allow resolution of genome diversification over shorter time periods. We have sequenced the genome of the strain wBol1-b, found in the butterfly Hypolimnas bolina, which kills the male offspring of infected hosts during embyronic development and is closely related to the non-male-killing strain wPip from Culex pipiens.ResultsThe genomes of wBol1-b and wPip are similar in genomic organisation, sequence and gene content, but show substantial differences at some rapidly evolving regions of the genome, primarily associated with prophage and repetitive elements. We identified 44 genes in wBol1-b that do not have homologs in any previously sequenced strains, indicating that Wolbachia’s non-core genome diversifies rapidly. These wBol1-b specific genes include a number that have been recently horizontally transferred from phylogenetically distant bacterial taxa. We further report a second possible case of horizontal gene transfer from a eukaryote into Wolbachia.ConclusionsOur analyses support the developing view that many endosymbiotic genomes are highly dynamic, and are exposed and receptive to exogenous genetic material from a wide range of sources. These data also suggest either that this bacterial species is particularly permissive for eukaryote-to-prokaryote gene transfers, or that these transfers may be more common than previously believed. The wBol1-b-specific genes we have identified provide candidates for further investigations of the genomic bases of phenotypic differences between closely-related Wolbachia strains.

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.…”

“…5-40% of arthropod species (Goodacre et al, 2006;Weinert et al, 2007;Duron et al, 2008a;Zug and Hammerstein, 2012). The constitution of their genomes is dynamic, with flexible gene content and rampant intra-generic recombination, indicating accelerated rates of diversification and adaptability (Wu et al, 2004;Klasson et al, 2008;Felsheim et al, 2009;Klasson et al, 2009;Gillespie et al, 2012;Penz et al, 2012;Duplouy et al, 2013). Remarkably, mobile genetic elements represent substantial fractions of these genomes (Bordenstein and Reznikoff, 2005;Wernegreen, 2005;Moran et al, 2008) as exemplified with insertion sequences (ISs), a group of genetically compact transposable elements encoding no functions other than an enzyme that catalyzes their own transposition (Felsheim et al, 2009;Cerveau et al, 2011b).…”

Birth of a W sex chromosome by horizontal transfer ofWolbachiabacterial symbiont genome

“…Of the latter, the 88 genes with <80% mapped nucleotides were considered severely truncated and likely nonfunctional in the f element. Wolbachia core genes absent or nonfunctional in the f element were identified using similarity searches by blastp against the 654 genes of the Wolbachia core genome (46). Of the 331 genes lacking or severely truncated in the f element, 85 belong to the Wolbachia core genome (based on >75% amino acid similarity and >80% alignment length to a Wolbachia core gene, using wPipPel as a reference).…”

Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator

“…This capacity to recombine likely constitutes a key mechanism for adaptation within an arthropod host, as advantageous alleles that arise through recombination could be rapidly fixed and spread through horizontal transmission. Moreover, horizontal gene transfer between distinct Wolbachia types also appears to be frequent (Baldo et al, 2005(Baldo et al, , 2006aDuplouy et al, 2013). Such process may give rise to advantageous genetic variants and reduce the accumulation of mildly deleterious mutations due to Muller's ratchet (Raychoudhury et al, 2009).…”