Abstract
Intracellular Wolbachia bacteria manipulate arthropod reproduction to promote their own inheritance. The most prevalent mechanism, cytoplasmic incompatibility (CI), traces to a Wolbachia deubiquitylase, CidB, and CidA. CidB has properties of a toxin, while CidA binds CidB and rescues embryonic viability. CidB is also toxic to yeast where we identified both host effects and high-copy suppressors of toxicity. The strongest suppressor was karyopherin-α, a nuclear-import receptor; this required nuclear localization-signal binding. A protein-interaction screen of Drosophila extracts using a substrate-trapping catalytic mutant, CidB*, also identified karyopherin-α; the P32 protamine-histone exchange factor bound as well. When CidB* bound CidA, these host protein interactions disappeared. These associations would place CidB at the zygotic male pronucleus where CI defects first manifest. Overexpression of karyopherin-α, P32, or CidA in female flies suppressed CI. We propose that CidB targets nuclear-protein import and protamine-histone exchange and that CidA rescues embryos by restricting CidB access to its targets.
Highlights
Wolbachia are obligate intracellular bacteria infecting arthropods and filarial nematodes (Werren et al, 2008)
We determined whether yeast host background altered toxicity of CidBwPip and tested other Wolbachia cytoplasmic incompatibility (CI) toxins for growth inhibition
The Wolbachia CidA and CidB proteins were recently found to be central to CI, but no CidB targets were known
Summary
Wolbachia are obligate intracellular bacteria infecting arthropods and filarial nematodes (Werren et al, 2008). They promote their maternal transmission by reproductive manipulations, most commonly cytoplasmic incompatibility (CI) (Beckmann et al, 2019a; Beckmann and Fallon, 2013; Beckmann et al, 2017; Chen et al, 2019). If females have matching infections, embryo viability is normal (Poinsot et al, 2003). It is a gene drive mechanism that selects for infected females. CI is being applied in mosquito control to sterilize mosquitoes (Bushland et al, 1955; Laven, 1967b; Mains et al, 2016; Zheng et al, 2019) and as a population replacement tool harnessing Wolbachia’s ability to inhibit infectious agents such as dengue and Zika viruses (Turelli and Hoffmann, 1991; Schmidt et al, 2017; Walker et al, 2011)
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