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High anti-viral protection without immune upregulation after interspecies Wolbachia transfer
Publication . Chrostek, Ewa; Marialva, Marta S P; Yamada, Ryuichi; O'Neill, Scott L; Teixeira, Luis
Wolbachia, endosymbionts that reside naturally in up to 40-70% of all insect species, are some of the most prevalent intracellular bacteria. Both Wolbachia wAu, naturally associated with Drosophila simulans, and wMel, native to Drosophila melanogaster, have been previously described to protect their hosts against viral infections. wMel transferred to D. simulans was also shown to have a strong antiviral effect. Here we directly compare one of the most protective wMel variants and wAu in D. melanogaster in the same host genetic background. We conclude that wAu protects better against viral infections, it grows exponentially and significantly shortens the lifespan of D. melanogaster. However, there is no difference between wMel and wAu in the expression of selected antimicrobial peptides. Therefore, neither the difference in anti-viral effect nor the life-shortening could be attributed to the immune stimulation by exogenous Wolbachia. Overall, we prove that stable transinfection with a highly protective Wolbachia is not necessarily associated with general immune activation.
Mutualism Breakdown by Amplification of Wolbachia Genes
Publication . Chrostek, Ewa; Teixeira, Luis
Most insect species are associated with vertically transmitted endosymbionts. Because of the mode of transmission, the fitness of these symbionts is dependent on the fitness of the hosts. Therefore, these endosymbionts need to control their proliferation in order to minimize their cost for the host. The genetic bases and mechanisms of this regulation remain largely undetermined. The maternally inherited bacteria of the genus Wolbachia are the most common endosymbionts of insects, providing some of them with fitness benefits. In Drosophila melanogaster, Wolbachia wMelPop is a unique virulent variant that proliferates massively in the hosts and shortens their lifespan. The genetic bases of wMelPop virulence are unknown, and their identification would allow a better understanding of how Wolbachia levels are regulated. Here we show that amplification of a region containing eight Wolbachia genes, called Octomom, is responsible for wMelPop virulence. Using Drosophila lines selected for carrying Wolbachia with different Octomom copy numbers, we demonstrate that the number of Octomom copies determines Wolbachia titers and the strength of the lethal phenotype. Octomom amplification is unstable, and reversion of copy number to one reverts all the phenotypes. Our results provide a link between genotype and phenotype in Wolbachia and identify a genomic region regulating Wolbachia proliferation. We also prove that these bacteria can evolve rapidly. Rapid evolution by changes in gene copy number may be common in endosymbionts with a high number of mobile elements and other repeated regions. Understanding wMelPop pathogenicity and variability also allows researchers to better control and predict the outcome of releasing mosquitoes transinfected with this variant to block human vector-borne diseases. Our results show that transition from a mutualist to a pathogen may occur because of a single genomic change in the endosymbiont. This implies that there must be constant selection on endosymbionts to control their densities.
Wolbachia Variants Induce Differential Protection to Viruses in Drosophila melanogaster: A Phenotypic and Phylogenomic Analysis
Publication . Chrostek, Ewa; Marialva, Marta S. P.; Esteves, Sara S.; Weinert, Lucy A.; Martinez, Julien; Jiggins, Francis M.; Teixeira, Luis
Wolbachia are intracellular bacterial symbionts that are able to protect various insect hosts from viral infections. This tripartite interaction was initially described in Drosophila melanogaster carrying wMel, its natural Wolbachia strain. wMel has been shown to be genetically polymorphic and there has been a recent change in variant frequencies in natural populations. We have compared the antiviral protection conferred by different wMel variants, their titres and influence on host longevity, in a genetically identical D. melanogaster host. The phenotypes cluster the variants into two groups--wMelCS-like and wMel-like. wMelCS-like variants give stronger protection against Drosophila C virus and Flock House virus, reach higher titres and often shorten the host lifespan. We have sequenced and assembled the genomes of these Wolbachia, and shown that the two phenotypic groups are two monophyletic groups. We have also analysed a virulent and over-replicating variant, wMelPop, which protects D. melanogaster even better than the closely related wMelCS. We have found that a ~21 kb region of the genome, encoding eight genes, is amplified seven times in wMelPop and may be the cause of its phenotypes. Our results indicate that the more protective wMelCS-like variants, which sometimes have a cost, were replaced by the less protective but more benign wMel-like variants. This has resulted in a recent reduction in virus resistance in D. melanogaster in natural populations worldwide. Our work helps to understand the natural variation in wMel and its evolutionary dynamics, and inform the use of Wolbachia in arthropod-borne disease control.

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Wellcome Trust

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094664

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