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Cytoplasmic Incompatibility Variations in Relation with Genes Divergence in Culex Pipiens

Overview
Journal mBio
Specialty Microbiology
Date 2021 Feb 10
PMID 33563818
Citations 10
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Abstract

In arthropods, endosymbionts induce conditional sterility, called cytoplasmic incompatibility (CI), resulting from embryonic lethality. CI penetrance (i.e., embryonic death rate) varies depending on host species and strains involved. All mosquitoes are infected by the endosymbiotic alphaproteobacteria Pip. CI in , characterized as a binary "compatible/incompatible" phenomenon, revealed an unparalleled diversity of patterns linked to the amplification-diversification of and genes. Here, we accurately studied CI penetrance variations in the light of genes divergence by generating a compatibility matrix between 11 lines hosting different phylogenetic Pip groups and exhibiting distinct gene repertoires. We showed, as expected, that crosses involving Pip from the same group were mostly compatible. In contrast, only 22% of the crosses involving different Pip groups were compatible, while 54% were fully incompatible. For the remaining 24% of the crosses, "intermediate" compatibilities were reported, and a cytological observation of the first zygotic division confirmed the occurrence of "canonical" CI phenotypes in a fraction of the eggs. Backcross experiments demonstrated that intermediate compatibilities were not linked to host genetic background but to the strains involved. This previously unstudied intermediate penetrance CI was more severe and frequent in crosses involving Pip-IV strains exhibiting variants markedly divergent from other Pip groups. Our data demonstrate that CI is not always a binary compatible/incompatible phenomenon in but that intermediate compatibilities putatively resulting from partial mismatch due to Cid proteins divergence exist in this species complex. mosquitoes are infected with Pip. These endosymbionts induce a conditional sterility called CI resulting from embryonic deaths, which constitutes a cornerstone for antivectorial methods. Recent studies revealed that (i) two genes, and , are central in -CI mechanisms, and (ii) compatibility versus incompatibility between mosquito lines depends on the Pip phylogenetic groups at play. Here, we studied CI variations in relation to Pip groups and genes divergence. We showed, as expected, that the crosses involving Pip from the same group were compatible. In contrast, 78% of the crosses involving different Pip groups were partially or fully incompatible. In such crosses, we reported defects during the first zygotic division, a hallmark of CI. We showed that CI was more severe and frequent in crosses involving Pip-IV strains exhibiting variants, which markedly diverge from those of other Pip groups.

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References
1.
Bonneau M, Landmann F, Labbe P, Justy F, Weill M, Sicard M . The cellular phenotype of cytoplasmic incompatibility in Culex pipiens in the light of cidB diversity. PLoS Pathog. 2018; 14(10):e1007364. PMC: 6201942. DOI: 10.1371/journal.ppat.1007364. View

2.
Chen H, Zhang M, Hochstrasser M . The Biochemistry of Cytoplasmic Incompatibility Caused by Endosymbiotic Bacteria. Genes (Basel). 2020; 11(8). PMC: 7465683. DOI: 10.3390/genes11080852. View

3.
LePage D, Metcalf J, Bordenstein S, On J, Perlmutter J, Shropshire J . Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature. 2017; 543(7644):243-247. PMC: 5358093. DOI: 10.1038/nature21391. View

4.
Atyame C, Duron O, Tortosa P, Pasteur N, Fort P, Weill M . Multiple Wolbachia determinants control the evolution of cytoplasmic incompatibilities in Culex pipiens mosquito populations. Mol Ecol. 2010; 20(2):286-98. DOI: 10.1111/j.1365-294X.2010.04937.x. View

5.
Barr A . Cytoplasmic incompatibility as a means of eradication of Culex pipiens L. Proc Pap Annu Conf Calif Mosq Control Assoc. 1966; 34:32-5. View