Reactive Oxygen Species Production and Brugia pahangi Survivorship in Aedes polynesiensis with Artificial Wolbachia Infection Types

Abstract

Heterologous transinfection with the endosymbiotic bacterium Wolbachia has been shown previously to induce pathogen interference phenotypes in mosquito hosts. Here we examine an artificially infected strain of Aedes polynesiensis, the primary vector of Wuchereria bancrofti, which is the causative agent of Lymphatic filariasis (LF) throughout much of the South Pacific. Embryonic microinjection was used to transfer the wAlbB infection from Aedes albopictus into an aposymbiotic strain of Ae. polynesiensis. The resulting strain (designated “MTB”) experiences a stable artificial infection with high maternal inheritance. Reciprocal crosses of MTB with naturally infected wild-type Ae. polynesiensis demonstrate strong bidirectional incompatibility. Levels of reactive oxygen species (ROS) in the MTB strain differ significantly relative to that of the wild-type, indicating an impaired ability to regulate oxidative stress. Following a challenge with Brugia pahangi, the number of filarial worms achieving the infective stage is significantly reduced in MTB as compared to the naturally infected and aposymbiotic strains. Survivorship of MTB differed significantly from that of the wild-type, with an interactive effect between survivorship and blood feeding. The results demonstrate a direct correlation between decreased ROS levels and decreased survival of adult female Aedes polynesiensis. The results are discussed in relation to the interaction of Wolbachia with ROS production and antioxidant expression, iron homeostasis and the insect immune system. We discuss the potential applied use of the MTB strain for impacting Ae. polynesiensis populations and strategies for reducing LF incidence in the South Pacific.

The oxidative environment: a mediator of interspecies communication that drives symbiosis evolution

“…As this study focuses on an artificial infection, it is informative of the initial state of a Wolbachia-insect symbiosis: a state where the host immune response leads to a disruption of oxidative homeostasis. However, the evolution of tolerance through a reduction of ROS production may occur when the two partners coevolve [60]. Aedes polynesiensis is a naturally infected species in which Wolbachia infection is not associated with an increase in H 2 O 2 levels.…”

“…Aedes polynesiensis is a naturally infected species in which Wolbachia infection is not associated with an increase in H 2 O 2 levels. Indeed, ROS are equally produced in naturally infected and aposymbiotic (Wolbachia-free) mosquitoes [60]. By contrast, artificial injections of another Wolbachia strain in aposymbiotic mosquitoes increase H 2 O 2 levels [60].…”

Comparison of Stable and Transient Wolbachia Infection Models in Aedes aegypti to Block Dengue and West Nile Viruses

“…albopictus (cured of its natural Wolbachia infection and transinfected with the w Mel Wolbachia strain [12]), and Ae . polynesienses and Anopheles stephensi (both transinfected with the w AlbB Wolbachia strain [13, 14]). These transinfected strains have shown excellent potential for the biocontrol of several important mosquito-transmitted diseases (for recent reviews see [15–17]).…”

Metagenomics, paratransgenesis and the Anopheles microbiome: a portrait of the geographical distribution of the anopheline microbiota based on a meta-analysis of reported taxa

“…albopictus - Wolbachia ( w albA and w AlbB) (Armbruster et al 2003) and Aedes polynesiensis - Wolbachia ( w PolA) (Andrews et al 2012). Secondary symbionts may have more recently associated with their insect host and are thus not obligate, although they may fulfill a role in host biology (Minard et al 2013).…”