ANOTHER TOOL IN THE TOOLBOX: Wolbachia-mediated protection against a specialized fungal pathogen of aphids

Abstract

Aphids harbor nine heritable facultative symbionts, most mediating one or more ecological interactions. However, one aphid symbiont, Wolbachia, has eluded functional characterization despite being well-studied in other arthropods. In Pentalonia aphids, global pests of banana, Wolbachia was hypothesized to function as a co-obligate symbiont alongside the traditional obligate Buchnera, but subsequent genomic analyses failed to support this role. Sampling across multiple aphid populations, we found that > 80% of Pentalonia aphids carried a M-supergroup strain of Wolbachia named wPni. While the lack of fixation confirms that Wolbachia is not a co-obligate symbiont, the high infection frequencies in these entirely asexual aphids strongly suggested Wolbachia confers net fitness benefits. Finding no correlation between Wolbachia and aphid food plants use, we challenged Wolbachia-infected aphids with common natural enemies. While Wolbachia did not protect aphids against parasitoids, this symbiont conferred significant protection against the specialized fungal pathogen, Pandora neoaphidis, and improved aphid fitness in the absence of enemy challenge. Thus, we identified a new phenotype for the multifaceted Wolbachia and highlight a system that provides unique opportunities to merge key models of heritable symbiosis to better understand infection dynamics in nature and mechanisms underpinning symbiont-mediated phenotypes. IMPORTANCE: Wolbachia symbionts spread and persist in a wide range of arthropods and nematodes by using a range of functional strategies, including reproductive manipulation, providing protection against viral and bacterial pathogens or by provisioning nutrients. Despite being one of the best-studied symbionts, little is known about the strains that infect aphids. In this study, we characterized the functional role of a Supergroup M Wolbachia strain infecting strictly asexual aphids of the genus Pentalonia. We report for the first time that this symbiont also defends against fungal entomopathogens and expand on the range of phenotypes conferred by this multifaceted symbiont.