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A Role for Maternal Factors in Suppressing Cytoplasmic Incompatibility.

ABSTRACT: Wolbachia are maternally transmitted bacterial endosymbionts, carried by approximately half of all insect species. Wolbachia prevalence in nature stems from manipulation of host reproduction to favor the success of infected females. The best known reproductive modification induced by Wolbachia is referred to as sperm-egg Cytoplasmic Incompatibility (CI). In CI, the sperm of Wolbachia-infected males cause embryonic lethality, attributed to paternal chromatin segregation defects during early mitotic divisions. Remarkably, the embryos of Wolbachia-infected females "rescue" CI lethality, yielding egg hatch rates equivalent to uninfected female crosses. Several models have been discussed as the basis for Rescue, and functional evidence indicates a major contribution by Wolbachia CI factors. A role for host contributions to Rescue remains largely untested. In this study, we used a chemical feeding approach to test for CI suppression capabilities by Drosophila simulans. We found that uninfected females exhibited significantly higher CI egg hatch rates in response to seven chemical treatments that affect DNA integrity, cell cycle control, and protein turnover. Three of these treatments suppressed CI induced by endogenous wRi Wolbachia, as well as an ectopic wMel Wolbachia infection. The results implicate DNA integrity as a focal aspect of CI suppression for different Wolbachia strains. The framework presented here, applied to diverse CI models, will further enrich our understanding of host reproductive manipulation by insect endosymbionts.

SUBMITTER: Momtaz AZ

PROVIDER: S-EPMC7680759 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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A Role for Maternal Factors in Suppressing Cytoplasmic Incompatibility.

Momtaz Ajm Zehadee AZ Ahumada Sabagh Abraham D AD Gonzalez Amortegui Julian G JG Salazar Samuel A SA Finessi Andrea A Hernandez Jethel J Christensen Steen S Serbus Laura R LR

Frontiers in microbiology 20201109

Wolbachia are maternally transmitted bacterial endosymbionts, carried by approximately half of all insect species. Wolbachia prevalence in nature stems from manipulation of host reproduction to favor the success of infected females. The best known reproductive modification induced by Wolbachia is referred to as sperm-egg Cytoplasmic Incompatibility (CI). In CI, the sperm of Wolbachia-infected males cause embryonic lethality, attributed to paternal chromatin segregatio ...[more]

PMID: 33240234

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Project description:BackgroundThe endosymbiont Wolbachia can manipulate arthropod reproduction and invade host populations by inducing cytoplasmic incompatibility (CI). Some host species are coinfected with multiple Wolbachia strains which may have sequentially invaded host populations by expressing different types of modular CI factor (cif) genes. The tephritid fruit fly Rhagoletis cerasi is a model for CI and Wolbachia population dynamics. It is associated with at least four Wolbachia strains in various combinations, with demonstrated (wCer2, wCer4), predicted (wCer1) or unknown (wCer5) CI phenotypes.ResultsWe sequenced and assembled the draft genomes of the Wolbachia strains wCer1, wCer4 and wCer5, and compared these with the previously sequenced genome of wCer2 which currently invades R. cerasi populations. We found complete cif gene pairs in all strains: four pairs in wCer2 (three Type I; one Type V), two pairs in wCer1 (both Type I) and wCer4 (one Type I; one Type V), and one pair in wCer5 (Type IV). Wolbachia genome variant analyses across geographically and genetically distant host populations revealed the largest diversity of single nucleotide polymorphisms (SNPs) in wCer5, followed by wCer1 and then wCer2, indicative of their different lengths of host associations. Furthermore, mitogenome analyses of the Wolbachia genome-sequenced individuals in combination with SNP data from six European countries revealed polymorphic mitogenome sites that displayed reduced diversity in individuals infected with wCer2 compared to those without.ConclusionsCoinfections with Wolbachia are common in arthropods and affect options for Wolbachia-based management strategies of pest and vector species already infected by Wolbachia. Our analyses of Wolbachia genomes of a host naturally coinfected by several strains unravelled signatures of the evolutionary dynamics in both Wolbachia and host mitochondrial genomes as a consequence of repeated invasions. Invasion of already infected populations by new Wolbachia strains requires new sets of functionally different cif genes and thereby may select for a cumulative modularity of cif gene diversity in invading strains. Furthermore, we demonstrated at the mitogenomic scale that repeated CI-driven Wolbachia invasions of hosts result in reduced mitochondrial diversity and hitchhiking effects. Already resident Wolbachia strains may experience similar cytoplasmic hitchhiking effects caused by the invading Wolbachia strain.

Dataset Information

A Role for Maternal Factors in Suppressing Cytoplasmic Incompatibility.

Publications

A Role for Maternal Factors in Suppressing Cytoplasmic Incompatibility.

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