Wolbachia-Associated Bacterial Protection in the Mosquito Aedes aegypti

Abstract

Background Wolbachia infections confer protection for their insect hosts against a range of pathogens including bacteria, viruses, nematodes and the malaria parasite. A single mechanism that might explain this broad-based pathogen protection is immune priming, in which the presence of the symbiont upregulates the basal immune response, preparing the insect to defend against subsequent pathogen infection. A study that compared natural Wolbachia infections in Drosophila melanogaster with the mosquito vector Aedes aegypti artificially transinfected with the same strains has suggested that innate immune priming may only occur in recent host-Wolbachia associations. This same study also revealed that while immune priming may play a role in viral protection it cannot explain the entirety of the effect.Methodology/FindingsHere we assess whether the level of innate immune priming induced by different Wolbachia strains in A. aegypti is correlated with the degree of protection conferred against bacterial pathogens. We show that Wolbachia strains wMel and wMelPop, currently being tested for field release for dengue biocontrol, differ in their protective abilities. The wMelPop strain provides stronger, more broad-based protection than wMel, and this is likely explained by both the higher induction of immune gene expression and the strain-specific activation of particular genes. We also show that Wolbachia densities themselves decline during pathogen infection, likely as a result of the immune induction.Conclusions/SignificanceThis work shows a correlation between innate immune priming and bacterial protection phenotypes. The ability of the Toll pathway, melanisation and antimicrobial peptides to enhance viral protection or to provide the basis of malaria protection should be further explored in the context of this two-strain comparison. This work raises the questions of whether Wolbachia may improve the ability of wild mosquitoes to survive pathogen infection or alter the natural composition of gut flora, and thus have broader consequences for host fitness.

The bacteriumWolbachiaexploits host innate immunity to establish a symbiotic relationship with the dengue vector mosquitoAedes aegypti

“…We observed that wAlbB protects WB1 mosquitoes from all three types of pathogen. This is in agreement with a previous report showing that both wMel and wMelPop can protect A. aegypti from infection with Gram-negative bacteria (Erwinia carotovora and Salmonella typhimurium), and wMelPop can increase survival of mosquitoes after challenge with Gram-positive bacteria (Mycobacterium marinum) (Ye et al, 2013). Thus, Wolbachiaboosted immunity is beneficial to the mosquito host owing to Wolbachia-associated protection against pathogens.…”

Insect-Specific Viruses Detected in Laboratory Mosquito Colonies and Their Potential Implications for Experiments Evaluating Arbovirus Vector Competence

“…[36][37][38][39][40] With the growing realization of the diversity of the mosquito microbiome, it is important to understand the nature of these microorganisms and the role they may play in vector ecology and arbovirus transmission. Few studies have been done to evaluate potential interactions between insectspecific viruses with arboviruses in mosquitoes.…”

Health and environmental applications of gut microbiome: a review

“…This broad-spectrum pathogen protection happens through immune priming that upregulates the basal immune response by inducing an array of reactions like cytoplasmic incompatibility (CI) in the presence of the symbiont and better preparing insects against subsequent infection by pathogens [30]. The similar kind of observation was found in transient infections established in the mosquito Anopheles gambiae [30,31]. Biocontrol strategy for reducing dengue virus transmission to humans may be achieved in future through the Wolbachia symbiont-infected mosquitoes [25].…”

“…It is also reported that when Plasmodium gallinaceum, a malaria parasite is stably transfected into Aedes aegypti mosquitoes, protection against the parasite is conferred [28,29]. This broad-spectrum pathogen protection happens through immune priming that upregulates the basal immune response by inducing an array of reactions like cytoplasmic incompatibility (CI) in the presence of the symbiont and better preparing insects against subsequent infection by pathogens [30]. The similar kind of observation was found in transient infections established in the mosquito Anopheles gambiae [30,31].…”

“…Biocontrol strategy for reducing dengue virus transmission to humans may be achieved in future through the Wolbachia symbiont-infected mosquitoes [25]. Bacteria like, Wolbachia, have an important role that modifies host fitness either by improving the ability of wild mosquitoes to survive pathogen infection or may alter the natural composition of gut flora that hinder the pathogen form colonization [30].…”