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Comparative Genomics of a Parthenogenesis-Inducing Wolbachia Symbiont.

ABSTRACT: Wolbachia is an intracellular symbiont of invertebrates responsible for inducing a wide variety of phenotypes in its host. These host-Wolbachia relationships span the continuum from reproductive parasitism to obligate mutualism, and provide a unique system to study genomic changes associated with the evolution of symbiosis. We present the genome sequence from a parthenogenesis-inducing Wolbachia strain (wTpre) infecting the minute parasitoid wasp Trichogramma pretiosum The wTpre genome is the most complete parthenogenesis-inducing Wolbachia genome available to date. We used comparative genomics across 16 Wolbachia strains, representing five supergroups, to identify a core Wolbachia genome of 496 sets of orthologous genes. Only 14 of these sets are unique to Wolbachia when compared to other bacteria from the Rickettsiales. We show that the B supergroup of Wolbachia, of which wTpre is a member, contains a significantly higher number of ankyrin repeat-containing genes than other supergroups. In the wTpre genome, there is evidence for truncation of the protein coding sequences in 20% of ORFs, mostly as a result of frameshift mutations. The wTpre strain represents a conversion from cytoplasmic incompatibility to a parthenogenesis-inducing lifestyle, and is required for reproduction in the Trichogramma host it infects. We hypothesize that the large number of coding frame truncations has accompanied the change in reproductive mode of the wTpre strain.

SUBMITTER: Lindsey AR

PROVIDER: S-EPMC4938664 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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Comparative Genomics of a Parthenogenesis-Inducing Wolbachia Symbiont.

Lindsey Amelia R I AR Werren John H JH Richards Stephen S Stouthamer Richard R

G3 (Bethesda, Md.) 20160707 7

Wolbachia is an intracellular symbiont of invertebrates responsible for inducing a wide variety of phenotypes in its host. These host-Wolbachia relationships span the continuum from reproductive parasitism to obligate mutualism, and provide a unique system to study genomic changes associated with the evolution of symbiosis. We present the genome sequence from a parthenogenesis-inducing Wolbachia strain (wTpre) infecting the minute parasitoid wasp Trichogramma pretiosum The wTpre genome is the mo ...[more]

PMID: 27194801

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Project description:BackgroundThe maternally inherited, bacterial symbiont, parthenogenesis inducing (PI) Wolbachia, causes females in some haplodiploid insects to produce daughters from both fertilized and unfertilized eggs. The symbionts, with their maternal inheritance, benefit from inducing the production of exclusively daughters, however the optimal sex ratio for the nuclear genome is more male-biased. Here we examine through models how an infection with PI-Wolbachia in a previously uninfected population leads to a genomic conflict between PI-Wolbachia and the nuclear genome. In most natural populations infected with PI-Wolbachia the infection has gone to fixation and sexual reproduction is impossible, specifically because the females have lost their ability to fertilize eggs, even when mated with functional males.ResultsThe PI Wolbachia infection by itself does not interfere with the fertilization process in infected eggs, fertilized infected eggs develop into biparental infected females. Because of the increasingly female-biased sex ratio in the population during a spreading PI-Wolbachia infection, sex allocation alleles in the host that cause the production of more sons are rapidly selected. In haplodiploid species a reduced fertilization rate leads to the production of more sons. Selection for the reduced fertilization rate leads to a spread of these alleles through both the infected and uninfected population, eventually resulting in the population becoming fixed for both the PI-Wolbachia infection and the reduced fertilization rate. Fertilization rate alleles that completely interfere with fertilization ("virginity alleles") will be selected over alleles that still allow for some fertilization. This drives the final resolution of the conflict: the irreversible loss of sexual reproduction and the complete dependence of the host on its symbiont.ConclusionsThis study shows that dependence among organisms can evolve rapidly due to the resolution of the conflicts between cytoplasmic and nuclear genes, and without requiring a mutualism between the partners.

Project description:Intersex is an intermediate stage of sexual differentiation in insects. Determining intersex morphology and the cause of its production will aid in the understanding of the mechanism of sexual differentiation in insects. In this paper, Wolbachia-infected Trichogramma pretiosum (T. preW+ ) that shows thelytokous parthenogenesis were used as subjects. In order to determine the causes of the T. preW+ intersex and the influence of parental generation temperature on gradual changes in secondary masculinization in intersex offspring, we examined the occurrence of intersex offspring (F1 and F2 generation) after the parental generations were treated with high temperature (27, 29, 31, and 33 °C) and described the external morphology of the intersexes. The results showed that the T. preW+ parental generation temperature is positively correlated with the probability of intersex offspring. The probability of F1 intersex is significantly higher than that of F2 intersex in different high temperature. The degree of secondary masculinization in T. preW+ intersexes increases as parental generation temperature increases. In addition, our study first identified 11 intersex types in T. preW+ and found that the primary and secondary sexual characteristics showed a regular distribution. We also found that the D type and H type of intersex have the highest frequency of appearance. The external genitalia of most intersexes were female, and only three intersex types have male external genitalia. Conclusions were ultimately obtained: Wolbachia is a direct factor that causes the occurrence of intersexes, while high temperature is an indirect factor that determines the external morphology of intersexes. The effects of high temperature on T. preW+ intersexes is passed through the parental generation to offspring, and this maternal effect weakens as the number of generations increases. In T. preW+ intersex individuals, most exhibit female primary sexual characteristics, and secondary sexual characteristics exhibit signs of masculinization.

Project description:The importance of host-specialization to speciation processes in obligate host-associated bacteria is well known, as is also the ability of recombination to generate cohesion in bacterial populations. However, whether divergent strains of highly recombining intracellular bacteria, such as Wolbachia, can maintain their genetic distinctness when infecting the same host is not known. We first developed a protocol for the genome sequencing of uncultivable endosymbionts. Using this method, we have sequenced the complete genomes of the Wolbachia strains wHa and wNo, which occur as natural double infections in Drosophila simulans populations on the Seychelles and in New Caledonia. Taxonomically, wHa belong to supergroup A and wNo to supergroup B. A comparative genomics study including additional strains supported the supergroup classification scheme and revealed 24 and 33 group-specific genes, putatively involved in host-adaptation processes. Recombination frequencies were high for strains of the same supergroup despite different host-preference patterns, leading to genomic cohesion. The inferred recombination fragments for strains of different supergroups were of short sizes, and the genomes of the co-infecting Wolbachia strains wHa and wNo were not more similar to each other and did not share more genes than other A- and B-group strains that infect different hosts. We conclude that Wolbachia strains of supergroup A and B represent genetically distinct clades, and that strains of different supergroups can co-exist in the same arthropod host without converging into the same species. This suggests that the supergroups are irreversibly separated and that barriers other than host-specialization are able to maintain distinct clades in recombining endosymbiont populations. Acquiring a good knowledge of the barriers to genetic exchange in Wolbachia will advance our understanding of how endosymbiont communities are constructed from vertically and horizontally transmitted genes.

Dataset Information

Comparative Genomics of a Parthenogenesis-Inducing Wolbachia Symbiont.

Publications

Comparative Genomics of a Parthenogenesis-Inducing Wolbachia Symbiont.

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