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.

Highlights

  • Lymphatic filariasis (LF) affects 120 million people globally and has been a leading cause of morbidity in South Pacific regions [1]

  • Because of inherent issues associated with mass drug administration (MDA), such as efficacy of antifilarial drugs and public compliance with drug regimens, an integrated approach that targets the vector has been suggested for the successful control of LF in some regions, such as the South Pacific

  • In this study we were able to successfully infect Ae. polynesiensis with an artificial Wolbachia type that is stably maintained and causes bidirectional cytoplasmic incompatibility when crossed with the wild-type strain

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Summary

Introduction

Lymphatic filariasis (LF) affects 120 million people globally and has been a leading cause of morbidity in South Pacific regions [1]. Aedes polynesiensis is the primary vector of Wuchereria bancrofti, the filarial nematode that causes LF in the South Pacific [2]. This mosquito is naturally infected with Wolbachia, a maternally inherited endosymbiont that infects a broad range of invertebrates [3,4]. Public health strategies under development are based upon manipulating Wolbachia induced CI in important mosquito species, either to suppress the population through releases of incompatible males or to harness CI as a gene-drive mechanism for spreading useful phenotypes, such as disease resistance, into a targeted population [5,6,7]. A recent proof of concept for this approach comes from a program in Australia that has successfully replaced an existing Ae. aegypti population with an artificially infected mosquito [8,9]

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