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The Mosaic Genome Structure of the Wolbachia Wri Strain Infecting Drosophila Simulans

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The Mosaic Genome Structure of the Wolbachia Wri Strain Infecting Drosophila Simulans The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans Lisa Klassona,1, Joakim Westberga,1, Panagiotis Sapountzisb, Kristina Na¨ slunda, Ylva Lutnaesa, Alistair C. Darbya,2, Zoe Venetic, Lanming Chend,3, Henk R. Braige, Roger Garrettd, Kostas Bourtzisb,c, and Siv G. E. Anderssona,4 aDepartment of Molecular Evolution, Evolutionary Biology Centre, Uppsala University, SE-752 36 Uppsala, Sweden; bDepartment of Environmental and Natural Resources Management, University of Ioannina, 30100 Agrinio, Greece; cInstitute of Molecular Biology and Biotechnology, FORTH, 71110 Heraklion, Crete, Greece; dCentre for Comparative Genomics, Department of Biology, University of Copenhagen, DK-2200 Copenhagen N, Denmark; and eSchool of Biological Sciences, Bangor University, Wales, LL57 2UW, United Kingdom Edited by Nancy A. Moran, University of Arizona, Tucson, AZ, and approved February 20, 2009 (received for review October 24, 2008) The obligate intracellular bacterium Wolbachia pipientis infects (7) are both reproductive parasites that cause CI, whereas the around 20% of all insect species. It is maternally inherited and D-group strain wBm is an obligate mutualist in the nematode induces reproductive alterations of insect populations by male Brugia malayi (8). The 1.27-Mb genome of wMel and the killing, feminization, parthenogenesis, or cytoplasmic incompati- 1.48-Mb genome of wPip contain several prophages and high bility. Here, we present the 1,445,873-bp genome of W. pipientis frequencies of repeated sequences, including many IS-elements. strain wRi that induces very strong cytoplasmic incompatibility in These genomes have a large repertoire of genes with ankyrin its natural host Drosophila simulans. A comparison with the pre- repeat motifs, 23 in wMel and 60 in wPip, several of which are viously sequenced genome of W. pipientis strain wMel from associated with mobile elements (6, 7). In contrast, the 1.08-Mb Drosophila melanogaster identified 35 breakpoints associated with genome of strain wBm contains no prophage, only a few ankyrin mobile elements and repeated sequences that are stable in Dro- repeat genes and a much lower fraction of repeated sequences, sophila lines transinfected with wRi. Additionally, 450 genes with possibly reflecting its mutualistic adaptation to a single-host orthologs in wRi and wMel were sequenced from the W. pipientis species. strain wUni, responsible for the induction of parthenogenesis in Sequence comparisons of single genes from multiple strains EVOLUTION the parasitoid wasp Muscidifurax uniraptor. The comparison of have provided evidence for recombination (9–12) and horizontal these A-group Wolbachia strains uncovered the most highly re- transfer of prophages and insertion sequence (IS)-elements combining intracellular bacterial genomes known to date. This was across Wolbachia strains (13–16). However, the distant relation- manifested in a 500-fold variation in sequence divergences at ship of the 3 sequenced Wolbachia genomes, manifested as an synonymous sites, with different genes and gene segments sup- almost complete lack of gene-order conservation and synony- porting different strain relationships. The substitution-frequency profile resembled that of Neisseria meningitidis, which is charac- mous substitution frequencies that are close to saturation, has terized by rampant intraspecies recombination, rather than that of precluded attempts to infer patterns and rates of recombination Rickettsia, where genes mostly diverge by nucleotide substitu- at the whole-genome level. Thus, with the exception of a few tions. The data further revealed diversification of ankyrin repeat single-gene studies, the extent to which recombination distorts genes by short tandem duplications and provided examples of the evolutionary coherence of Wolbachia genomes is currently horizontal gene transfer across A- and B-group strains that infect unknown. D. simulans. These results suggest that the transmission dynamics We report here the complete genome sequence of the super- of Wolbachia and the opportunity for coinfections have created a group-A Wolbachia strain wRi that naturally infects Drosophila freely recombining intracellular bacterial community with mosaic simulans and induces almost complete CI in its host (17, 18). genomes. Additionally, we present partial genome data of Wolbachia strain wUni from Muscidifurax uniraptor, likewise a supergroup-A horizontal transfer ͉ recombination ͉ ankyrin repeat gene ͉ strain that induces parthenogenesis in its host (19). A compar- genome evolution ͉ insect symbiosis ison of these 2 A-group Wolbachia strains with the previously sequenced genome of the A-group strain wMel reveals the most Wolbachia pipientis are intracellular ␣-proteobacteria of the highly recombining obligate intracellular bacterial community order Rickettsiales that infect insects as well as isopods, spiders, examined to date. scorpions, mites, and filarial nematodes (1, 2). These bacteria represent a single species, with strains classified into super- groups, of which the most abundant are supergroups A and B. Author contributions: H.R.B., R.G., K.B., and S.G.E.A. designed research; L.K., J.W., P.S., K.N., Y.L., A.C.D., Z.V., and L.C. performed research; L.K., J.W., K.B., and S.G.E.A. analyzed data; A lack of concordance between host and bacterial strain phy- and L.K., J.W., R.G., K.B., and S.G.E.A. wrote the paper. logenies indicate frequent host shifts in addition to maternal The authors declare no conflict of interest. inheritance within the individual host (1–4). In insect popula- tions, Wolbachia induce reproductive manipulations to enhance This article is a PNAS Direct Submission. their own spreading. The most frequently observed reproductive Freely available online through the PNAS open access option. abnormality is cytoplasmic incompatibility (CI) (1, 2, 5), where Data deposition: The sequences described in this paper have been deposited in GenBank database [accession nos. CP001391 (W. pipientis wRi) and ACFP01000000 (Wolbachia uninfected females are unable to produce offspring with infected wUni); the version described in this article is ACFP01000000]. males, whereas infected females can produce offspring with both 1L.K. and J.W. contributed equally to this work. infected and uninfected males, thus creating a reproductive 2Present address: School of Biological Sciences, University of Liverpool, Liverpool L69 7ZB, advantage for infected females. Other spectacular effects of United Kingdom. Wolbachia infections are male embryo killing, feminization, and 3Present address: School of Applied Sciences, University of Wolverhampton, Wolverhamp- parthenogenesis induction (1, 2). ton WV1 1LY, United Kingdom. Three genomes of Wolbachia have been published to date. The 4To whom correspondence should be addressed. E-mail: [email protected]. A-group strain wMel from Drosophila melanogaster (6) and the This article contains supporting information online at www.pnas.org/cgi/content/full/ B-group strain wPip from the mosquito Culex quinquefasciatus 0810753106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0810753106 PNAS Early Edition ͉ 1of6 Downloaded by guest on September 30, 2021 1 are located within or flanked by prophage sequences, and 6 are flanked by long repeats. The final breakpoint contains a 22-bp hairpin structure with a 4-bp loop. Among these breakpoints, 6 1,260,000 180,000 are close to genes encoding reverse trancriptase and 3 to genes A encoding DNA recombinase. This shows that mobile genetic elements and repeated sequences are hot spots for rearrange- ments in Wolbachia. To examine the stability of these recombi- nation hot spots, we used PCR to analyze all breakpoints from genomic DNA of wRi isolated from naturally infected and Wolbachia pipientis transinfected symbiotic associations of D. simulans, Drosophila 1,080,000 B strain wRi 360,000 yakuba, Drosophila teisseiri, and Drosophila santomea, which have 1,445,873 bp been kept in laboratory conditions from 8 to 15 years (Table S7). The results of this survey showed that the wRi genome remains stable in structure over these sites and suggests that the wRi genome does not oscillate between different genomic structures, B nor do host switches trigger rearrangements at these sites. The C observed short-term stability indicates that the recombination 900,000 540,000 frequencies at these repeated sequences are lower than could be detected over this time period. 720,000 The A-Group Wolbachia Strains are Evolutionary Genome Mosaics. We estimated the nonsynonymous (Ka) and synonymous (Ks) sub- Fig. 1. Circular map of the Wolbachia pipientis wRi genome. Each circle stitution frequency per site to quantify sequence divergences confined by the gray lines except for the 2 innermost circles illustrates differ- across strains, although these values may not correspond to ent features on the plus (outer region) and minus (inner region) strands. Lines and boxes in the 3 outermost circles are colored according to the Clusters of actual substitutions if genes evolve mainly by recombination. For Orthologous Groups (COG) categories. First (Outer) circle: protein-coding 851 positional homologs in the wRi and wMel genomes identified genes (CDSs). Second circle: pseudogenes. Third circle: unique CDSs compared by reciprocal BLAST searches (excluding phage genes), the Ϫ3 to wMel. Fourth circle: ANK genes in blue and gene synteny breakpoints median Ka and Ks values were estimated to be 6.2 ϫ 10 and Ϫ compared to wMel in red. Fifth circle: prophage
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