Many arthropod species carry maternally transmitted bacterial symbionts that manipulate host reproduction. Cytoplasmic incompatibility (CI), the most common reproductive manipulation, selectively kills embryonic offspring produced when infected males mate with uninfected females. Symbionts from several different bacterial phyla can cause CI as a result of convergent evolution. Currently, most knowledge on CI mechanisms comes from the Pseudomonadota symbiont Wolbachia, and from study of the widespread Wolbachia CI effector (cif) genes. However, little is known about the CI mechanisms of symbionts from different phyla in which cif genes are absent. Here, we identify two putative CI effector proteins of the Bacteroidota symbiont Cardinium hertigii cEper1 associated with the parasitoid wasp Encarsia suzannae. In previous work, we identified the pupal testes as the developmental stage and tissue in which a potentially lethal sperm modification occurs. Using proteomics, we compared symbiont gene expression across host sex, developmental stage, tissues, and symbiont secretome enrichments to identify candidate CI effector proteins. We heterologously expressed five candidates in yeast to assess their toxic potential. We show that two proteins, CAHE_0406 and CAHE_p0043, impaired yeast growth similar to the CI inducing proteins from Wolbachia (CidB). We identified homologs of CAHE_0406 and CAHE_p0043 in other Cardinium strains, and two of the CAHE_0406 homologs impaired yeast growth. These results suggest that CAHE_0406 and/or CAHE_p0043 could play a role in CI induction by Cardinium cEper1, and that the functions of CAHE_0406 may be conserved across some Cardinium lineages. These two Cardinium CI effector candidates share no similarity with known Wolbachia CI effectors, and these as well as other putative host-interaction proteins identified from Cardinium provide a new and broader perspective on the evolution of cytoplasmic incompatibility across bacterial lineages.
Mathieson, O. L., Schultz, D. L., Doremus, M. R., Vintila, S., Kelly, S. E., Hunter, M. S., Schmitz-Esser, S., Kleiner, M.
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