The nature of the immune response in novel Wolbachia-host associations

Abstract

Wolbachia is an obligate, intracellular symbiont that is commonly found in insects and causes a diverse array of reproductive manipulations. Normally transmitted vertically, the occasional horizontal host species jump can be seen in the lack of concordance between Wolbachia and host phylogenies. In the laboratory, the symbiont can be artificially introduced into novel hosts and selected to produce persistent infections. In the case of the vector of dengue virus, Aedes aegypti, the symbiont was successfully introduced with the aim of developing the bacterium for biocontrol. In this insect and others, Wolbachia limits co-infection with pathogens including viruses, bacteria and parasites. Here we have novelly infected cell lines derived from diverse insect species with Wolbachia in an attempt to determine if there are commonalities in the early host response to the symbiont. We then monitored the expression of genes in the antibacterial Toll and Imd pathways in the first several passages. We focused on immunity gene expression as it underpins the bulk of the transcriptional response to Wolbachia and because it may play a role in the pathogen blocking effect. We found that successful cell infections of Wolbachia were difficult to achieve and often required repeated rounds of reinfection. We saw significant variation in the nature of the transcriptional changes across cell lines and no attenuation of gene expression changes in the first several passages. These results suggest that insect species are likely to exhibit distinct responses to Wolbachia infection. They also reveal that any evolution of an attenuated transcriptional response, as predicted by long-standing Wolbachia x host associations, is not likely to occur rapidly. The findings will have implications for biocontrol programs that rely on the novel infection of naive hosts.