Lindsey, A. R. | bioRxiv Science

bioRxiv2023

Identification of parthenogenesis-inducing effector proteins in Wolbachia

Bacteria in the genus Wolbachia have evolved numerous strategies to manipulate arthropod sex, including the conversion of would-be male offspring to asexually reproducing females. This so-called "parthenogenesis-induction" phenotype can be found in a number of Wolbachia strains that infect arthropods with haplodiploid sex determination systems, including parasitoid wasps. Despite the discovery of microbe-mediated parthenogenesis more than 30 years ago, the underlying genetic mechanisms have remained elusive. We used a suite of genomic, computational, and molecular tools to identify and characterize two proteins that are uniquely found in parthenogenesis-inducing Wolbachia and have strong signatures of host-associated bacterial effector proteins. These putative parthenogenesis-inducing proteins have structural homology to eukaryotic protein domains including nucleoporins, the key insect sex-determining factor Transformer, and a eukaryotic-like serine-threonine kinase with leucine rich repeats. Furthermore, these proteins significantly impact eukaryotic cell biology in the model, Saccharomyces cerevisiae. We suggest these proteins are parthenogenesis-inducing factors and our results indicate this would be made possible by a novel mechanism of bacterial-host interaction.

evolutionary biology↗

bioRxiv2023

Wolbachia is a nutritional symbiont

The intracellular bacterium Wolbachia is a common symbiont of many arthropods and nematodes, well studied for its impacts on host reproductive biology. However, its broad success as a vertically transmitted infection cannot be attributed to manipulations of host reproduction alone. Using the Drosophila melanogaster model and their natively associated Wolbachia strain "wMel", we show that Wolbachia infection supports fly development and buffers against nutritional stress. Wolbachia infection across several fly genotypes and a range of nutrient conditions resulted in reduced pupal mortality, increased adult emergence, and larger size. We determined that the exogenous supplementation of pyrimidines partially rescued developmental phenotypes in the Wolbachia-free flies, and that Wolbachia titers were responsive to reduced gene expression of the flys de novo pyrimidine synthesis pathway. In parallel, transcriptomic and metabolomic analyses indicated that Wolbachia impacts larval biology far beyond pyrimidine metabolism. Wolbachia-infected larvae had strong signatures of shifts in glutathione and mitochondrial metabolism, plus significant changes in the expression of key developmental regulators including Notch, the insulin receptor (lnR), and the juvenile hormone receptor Methoprene-tolerant (Met). We propose that Wolbachia acts as a beneficial symbiont to support fly development and enhance host fitness, especially during periods of nutrient stress. SIGNIFICANCEWolbachia is a bacterial symbiont of arthropods and nematodes, well described for its manipulations of arthropod reproduction. However, many have theorized there must be more to this symbiosis, even in well-studied Wolbachia-host relationships such as with Drosophila. Reproductive impacts alone cannot explain the success and ubiquity of this bacterium. Here, we use Drosophila melanogaster and their native Wolbachia infections to show that Wolbachia supports fly development and significantly buffers flies against nutritional stress. These developmental advantages might help explain the ubiquity of Wolbachia infections.

developmental biology↗