The Wolbachia Genome of Brugia malayi: Endosymbiont Evolution within a Human Pathogenic Nematode

Molecular Parasitology Division, New England Biolabs, Beverly, Massachusetts, USA.
PLoS Biology (Impact Factor: 9.34). 05/2005; 3(4):e121. DOI: 10.1371/journal.pbio.0030121
Source: PubMed


Complete genome DNA sequence and analysis is presented for Wolbachia, the obligate alpha-proteobacterial endosymbiont required for fertility and survival of the human filarial parasitic nematode Brugia malayi. Although, quantitatively, the genome is even more degraded than those of closely related Rickettsia species, Wolbachia has retained more intact metabolic pathways. The ability to provide riboflavin, flavin adenine dinucleotide, heme, and nucleotides is likely to be Wolbachia's principal contribution to the mutualistic relationship, whereas the host nematode likely supplies amino acids required for Wolbachia growth. Genome comparison of the Wolbachia endosymbiont of B. malayi (wBm) with the Wolbachia endosymbiont of Drosophila melanogaster (wMel) shows that they share similar metabolic trends, although their genomes show a high degree of genome shuffling. In contrast to wMel, wBm contains no prophage and has a reduced level of repeated DNA. Both Wolbachia have lost a considerable number of membrane biogenesis genes that apparently make them unable to synthesize lipid A, the usual component of proteobacterial membranes. However, differences in their peptidoglycan structures may reflect the mutualistic lifestyle of wBm in contrast to the parasitic lifestyle of wMel. The smaller genome size of wBm, relative to wMel, may reflect the loss of genes required for infecting host cells and avoiding host defense systems. Analysis of this first sequenced endosymbiont genome from a filarial nematode provides insight into endosymbiont evolution and additionally provides new potential targets for elimination of cutaneous and lymphatic human filarial disease.

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Available from: Shiliang Wang
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    • "It has been observed that levels of genome synteny are higher within than between Wolbachia supergroups [30], as it is evidenced in Fig. 2 for ten finished genomes. Wolbachia genomes have high levels of repetitive DNA and mobile genetic elements that lead to DNA rearrangements that diminish synteny even between related strains [30] [35] [52] [102]. Genome rearrangements in other organisms represent recombination barriers and could lead to genetic isolation [76]. "
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    ABSTRACT: Wolbachia are highly extended bacterial endosymbionts that infect arthropods and filarial nematodes and produce contrasting phenotypes on their hosts. Wolbachia taxonomy has been understudied. Currently, Wolbachia strains are classified into phylogenetic supergroups. Here we applied phylogenomic analyses to study Wolbachia evolutionary relationships and examined metrics derived from their genome sequences such as average nucleotide identity (ANI), in silico DNA-DNA hybridization (DDH), G+C content, and synteny to shed light on the taxonomy of these bacteria. Draft genome sequences of strains wDacA and wDacB obtained from the carmine cochineal insect Dactylopius coccus were included. Although all analyses indicated that each Wolbachia supergroup represents a distinct evolutionary lineage, we found that some of the analyzed supergroups showed enough internal heterogeneity to be considered as assemblages of more than one species. Thus, supergroups would represent supraspecific groupings. Consequently, Wolbachia pipientis nomen species would apply only to strains of supergroup B and we propose the designation of 'Candidatus Wolbachia bourtzisii', 'Candidatus Wolbachia onchocercicola', 'Candidatus Wolbachia blaxterii', 'Candidatus Wolbachia brugii', 'Candidatus Wolbachia taylorii', 'Candidatus Wolbachia collembolicola' and 'Candidatus Wolbachia multihospitis' for other supergroups. Copyright © 2015 Elsevier GmbH. All rights reserved.
    Full-text · Article · Jul 2015 · Systematic and Applied Microbiology
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    • "The experimental/analytical techniques comprised a wide range including classical crossing and fecundity measurements (e.g., Hoffmann et al., 1990; Dunn et al., 2006), microscopic approaches (in situ hybridizations, electron microscope and immunohistochemical techniques for bacterium detection inside hosts and cells, tissues, etc.) (e.g., Negri et al., 2008; Fischer et al., 2011), gene expression analysis (e.g., Xi et al., September 2014 | Volume 5 | Article 430 | 1 2008; Kremer et al., 2009, 2012; Hughes et al., 2011; Chevalier et al., 2012; Darby et al., 2012; Liu et al., 2014), bioinformatic genome sequence annotation and functional prediction (e.g., Wu et al., 2004; Foster et al., 2005; Klasson et al., 2008), and mathematical modeling of the ecological consequences of CI or sex ratio distortion (e.g., Taylor, 1990; Turelli, 1994). Despite all these efforts, a coherent mechanistic story of Wolbachia's effect is still lacking. "
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    ABSTRACT: Wolbachia causes the feminization of chromosomally male embryos in several species of crustaceans and insects, including the leafhopper Zyginidia pullula. In contrast to the relatively well-established ecological aspects of male feminization (e.g., sex ratio distortion and its consequences), the underlying molecular mechanisms remain understudied and unclear. We embarked on an exploratory study to investigate the extent and nature of Wolbachia's effect on gene expression pattern in Z. pullula. We sequenced whole transcriptomes from Wolbachia-infected and uninfected adults. 18147 loci were assembled de novo, including homologs of several Drosophila sex determination genes. A number of transcripts were flagged as candidate Wolbachia sequences. Despite the resemblance of Wolbachia-infected chromosomal males to uninfected and infected chromosomal females in terms of sexual morphology and behavior, principal component analysis revealed that gene expression patterns did not follow these sexual phenotype categories. The principal components generated by differentially expressed genes specified a strong sex-independent Wolbachia effect, followed by a weaker Wolbachia-sexual karyotype interaction effect. Approaches to further examine the molecular mechanism of Wolbachia-host interactions have been suggested based on the presented findings.
    Full-text · Article · Sep 2014 · Frontiers in Microbiology
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    • "Shotgun sequencing of the wRec genome was conducted using an Illumina Hi-Seq (Vanderbilt Sequencing Core, Nashville, TN) with 100 bp paired end sequencing. Reads were filtered using five available Wolbachia genomes, wBm (Foster et al., 2005), wMel (Wu et al., 2004), wRi (Klasson et al., 2009), wOo (Darby et al., 2012), and wPip (Klasson et al., 2008), by mapping reads to these genomes with length and similarity fractions of 0.5 and keeping all mapped reads, using CLC Genomics Workbench version 6.0.4 (CLC Inc, Aarhus, Denmark). A de novo assembly with a length fraction of 0.5 and similarity fraction of 0.8 was then performed on filtered reads. "
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    ABSTRACT: Wolbachia are maternally transmitted endosymbionts that often alter their arthropod hosts' biology to favor the success of infected females, and they may also serve as a speciation microbe driving reproductive isolation. Two of these host manipulations include killing males outright and reducing offspring survival when infected males mate with uninfected females, a phenomenon known as cytoplasmic incompatibility. Little is known about the mechanisms behind these phenotypes, but interestingly ei-ther effect can be caused by the same Wolbachia strain when infecting different hosts. For instance, wRec causes cytoplasmic incompatibility in its native host Drosophila recens and male killing in D. subquinaria. The discovery of prophage WO elements in most arthropod Wolbachia has generated the hypothesis that WO may encode genes involved in these reproductive manipulations. However, PCR screens for the WO minor capsid gene indicated that wRec lacks phage WO. Thus, wRec seemed to provide an example where phage WO is not needed for Wolbachia-induced re-productive manipulation. To enable investigation of the mechanism of phenotype switching in different host backgrounds, and to examine the unexpected absence of phage WO, we sequenced the genome of wRec. Analyses reveal that wRec diverged from wMel approximately 350,000 years ago, mainly by genome reduction in the phage regions. While it lost the minor capsid gene used in standard PCR screens for phage WO, it retained two regions encompassing 33 genes, several of which have pre-viously been associated with reproductive parasitism. Thus, WO gene involvement in reproductive manipulation cannot be excluded and reliance on single gene PCR should not be used to rule out the presence of phage WO in Wolbachia. Additionally, the genome sequence for wRec will enable transcriptomic and proteomic studies that may help elucidate the Wolbachia mechanisms of altered reproductive manipulations associated with host switching, perhaps among the 33 remaining phage genes.
    Full-text · Article · Aug 2014 · PeerJ
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