Variation in Wolbachia cidB gene, but not cidA, is associated with cytoplasmic incompatibility mod phenotype diversity in Culex pipiens

Abstract

Endosymbiotic Wolbachia bacteria are, to date, considered the most widespread symbionts in arthropods and are the cornerstone of major biological control strategies. Such a high prevalence is based on the ability of Wolbachia to manipulate their hosts' reproduction. One manipulation called cytoplasmic incompatibility (CI) is based on the death of the embryos generated by crosses between infected males and uninfected females or between individuals infected with incompatible Wolbachia strains. CI can be seen as a modification‐rescue system (or mod‐resc) in which paternal Wolbachia produce mod factors, inducing embryonic defects, unless the maternal Wolbachia produce compatible resc factors. Transgenic experiments in Drosophila melanogaster and Saccharomyces cerevisiae converged towards a model where the cidB Wolbachia gene is involved in the mod function while cidA is involved in the resc function. However, as cidA expression in Drosophila males was required to observe CI, it has been proposed that cidA could be involved in both resc and mod functions. A recent correlative study in natural Culex pipiens mosquito populations has revealed an association between specific cidA and cidB variations and changes in mod phenotype, also suggesting a role for both these genes in mod diversity. Here, by studying cidA and cidB genomic repertoires of individuals from newly sampled natural C. pipiens populations harbouring wPipIV strains from North Italy, we reinforce the link between cidB variation and mod phenotype variation fostering the involvement of cidB in the mod phenotype diversity. However, no association between any cidA variants or combination of cidA variants and mod phenotype variation was observed. Taken together our results in natural C. pipiens populations do not support the involvement of cidA in mod phenotype variation.

Wolbachia pipientis Associated With Tephritid Fruit Fly Pests: From Basic Research to Applications

“…Several recent breakthrough studies have collectively identified Wolbachia-encoded genes (of viral origin) that contribute to the induction and rescue of CI (Beckmann et al, 2017;LePage et al, 2017;Bonneau et al, 2018Bonneau et al, , 2019Lindsey et al, 2018;Shropshire et al, 2018;Beckmann et al, 2019c;Chen et al, 2019;. Wolbachia-encoded genes that rescue CI are labeled as cifA, cidA, or cindA, depending on whether they rescue a defect caused by deubiquitylase (d), nuclease (n), both (nd); "f " is used by certain authors and/or when the nature of the defect is unknown (see Beckmann et al, 2019a,b;.…”

Symbiont-Mediated Cytoplasmic Incompatibility: What have we Learned in 50 Years?

“…Sequence divergence in CI-associated factors has long been thought to be a contributing factor to these incompatibilities, namely that divergence in both CI-causing and rescue-causing genes would be required for bidirectional CI to emerge (Charlat et al, 2001). Indeed, phylogenetic analyses of cif genes reveal that strains carrying similar alleles tend to be compatible, strains with more distantly related cif genes are not, and a single Wolbachia strain can have multiple unique cif gene pairs (Bonneau et al, 2018a(Bonneau et al, , 2019LePage et al, 2017). For instance, when wMel is transinfected into a D. simulans background, it is unidirectionally incompatible with the native wRi strain, wherein wRi can rescue wMel-induced CI but the reciprocal cross is incompatible (Poinsot et al, 1998).…”

“…Thus, it is plausible that wRi can rescue wMel's CI because of CifAwRi[T1] whereas wMel cannot rescue wRi's CI because it lacks a rescue gene for the Type 2 gene pair (LePage et al, 2017). Additionally, population genetic analyses of cif genes in wPip reveal that there are numerous unique strains, each strain carries multiple closely related cif variants that belong to Type 1 and Type 4 cif clades, and a single genetic variant of CifBwPip[T1] correlates with the inability of one strain of wPip to rescue CI caused by a divergent wPip strain (Atyame et al, 2011b;Bonneau et al, 2018aBonneau et al, , 2019. However, while these data suggest that cif genetic variation and/or copy number contributes to strain incompatibility, it remains possible that the considerable host genotypic variation between these incompatible populations contributes to these relationships in a way that also correlates with cif genotypic diversity (Atyame et al, 2011a).…”

“…This model leveraged predictions of the mod/resc model that (i) strains can have multiple sets of mod/lock and resc/key factors and that (ii) a key is more likely to bind to its associated lock than to a divergent lock. Indeed, Wolbachia exhibit considerable cif polymorphism (Bing et al, 2020;Bonneau et al, 2019;LePage et al, 2017;Lindsey et al, 2018) and binding of CifA and CifB is strongest between cognate partners (Beckmann et al, 2017). However, the lingering questions with the TA model also apply with the lock-and-key model.…”

<strong>Symbiont-mediated Cytoplasmic Incompatibility:</strong><strong>What Have We Learned in 50 years?</strong>

“…Thus, it is plausible that wRi can rescue wMel's CI because of CifAwRi[T1] whereas wMel cannot rescue wRi's CI because it lacks a rescue gene for the Type 2 gene pair (LePage et al, 2017). Additionally, population genetic analyses of cif genes in wPip reveal that there are numerous unique strains, each strain carries multiple closely related cif variants that belong to Type 1 and Type 4 cif clades, and a single genetic variant of CifBwPip[T1] correlates with the inability of one strain of wPip to rescue CI caused by a divergent wPip strain (Atyame et al, 2011b;Bonneau et al, 2018aBonneau et al, , 2019. However, while these data suggest that cif genetic variation and/or copy number contributes to strain incompatibility, it remains possible that the considerable host genotypic variation between these incompatible populations contributes to these relationships in a way that also correlates with cif genotypic diversity (Atyame et al, 2011a).…”