The cellular phenotype of cytoplasmic incompatibility in Culex pipiens in the light of cidB diversity

Manon Bonneau (1) , Frederic Landmann (2) , Pierrick Labbe (1) , Fabienne Justy (1) , Mylène Weill (1) , Mathieu Sicard (1)

1 UMR ISEM - Institut des Sciences de l'Evolution de Montpellier
2 CRBM - Centre de recherche en Biologie cellulaire de Montpellier

Wolbachia are maternally inherited endosymbiotic bacteria, widespread among arthropods thanks to host reproductive manipulations that increase their prevalence into host populations. The most commonly observed manipulation is cytoplasmic incompatibility (CI). CI leads to embryonic death in crosses between i) infected males and uninfected females and ii) individuals infected with incompatible Wolbachia strains. CI can be conceptualized as a toxin-antidote system where a toxin deposited by Wolbachia in the sperm would induce embryonic death unless countered by an antidote produced by Wolbachia present in the eggs. In Drosophila melanogaster, transgenic expression of Wolbachia effector cidB revealed its function of CI-inducing toxin. Moreover in Culex pipiens, the diversity of cidB variants present in wPip strains accounts for the diversity in crossing-types. We conducted cytological analyses to determine the CI mechanisms that lead to embryonic death in C. pipiens, and assess whether diversity in crossing-types could be based on variations in these mechanisms. We revealed that paternal chromatin condensation and segregation defects during the first embryonic division are always responsible for embryonic death. The strongest observed defects lead to an exclusion of the paternal chromatin from the first zygotic division, resulting in haploid embryos unable to hatch. The proportion of unhatched haploid embryos, developing with only maternal chromatin, which reflects the frequency of strong defects can be considered as a proxy of CI intensity at the cellular level. We thus studied the putative effect of variations in crossing types and cidB diversification on CI defects intensity. Incompatible crosses involving distinct wPip strains revealed that CI defects intensity depends on the Wolbachia strains hosted by the males and is linked to the diversity of cidB genes harbored in their genomes. These results support that, additionally to its implication in C. pipiens crossing type variability, cidB diversification also influences the strength of CI embryonic defects.

Domaines: Zoologie des invertébrés; Reproduction sexuée; Embryologie et organogenèse; Génétique animale

Manon Bonneau, Frederic Landmann, Pierrick Labbe, Fabienne Justy, Mylène Weill, et al.. The cellular phenotype of cytoplasmic incompatibility in Culex pipiens in the light of cidB diversity. PLoS Pathogens, 2018, 14 (10), pp.e1007364. ⟨10.1371/journal.ppat.1007364⟩. ⟨hal-01938013v2⟩