Dataset Information

Diet-Induced Nutritional Stress and Pathogen Interference in Wolbachia-Infected Aedes aegypti.

ABSTRACT: The pathogen interference phenotype greatly restricts infection with dengue virus (DENV) and other pathogens in Wolbachia-infected Aedes aegypti, and is a vital component of Wolbachia-based mosquito control. Critically, the phenotype's causal mechanism is complex and poorly understood, with recent evidence suggesting that the cause may be species specific. To better understand this important phenotype, we investigated the role of diet-induced nutritional stress on interference against DENV and the avian malarial parasite Plasmodium gallinaceum in Wolbachia-infected Ae. aegypti, and on physiological processes linked to the phenotype. Wolbachia-infected mosquitoes were fed one of four different concentrations of sucrose, and then challenged with either P. gallinaceum or DENV. Interference against P. gallinaceum was significantly weakened by the change in diet however there was no effect on DENV interference. Immune gene expression and H2O2 levels have previously been linked to pathogen interference. These traits were assayed for mosquitoes on each diet using RT-qPCR and the Amplex Red Hydrogen Peroxide/Peroxidase Assay Kit, and it was observed that the change in diet did not significantly affect immune expression, but low carbohydrate levels led to a loss of ROS induction in Wolbachia-infected mosquitoes. Our data suggest that host nutrition may not influence DENV interference for Wolbachia-infected mosquitoes, but Plasmodium interference may be linked to both nutrition and oxidative stress. This pathogen-specific response to nutritional change highlights the complex nature of interactions between Wolbachia and pathogens in mosquitoes.

SUBMITTER: Caragata EP

PROVIDER: S-EPMC5125575 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Diet-Induced Nutritional Stress and Pathogen Interference in Wolbachia-Infected Aedes aegypti.

Caragata Eric Pearce EP Rezende Fernanda Oliveira FO Simões Taynãna César TC Moreira Luciano Andrade LA

PLoS neglected tropical diseases 20161128 11

The pathogen interference phenotype greatly restricts infection with dengue virus (DENV) and other pathogens in Wolbachia-infected Aedes aegypti, and is a vital component of Wolbachia-based mosquito control. Critically, the phenotype's causal mechanism is complex and poorly understood, with recent evidence suggesting that the cause may be species specific. To better understand this important phenotype, we investigated the role of diet-induced nutritional stress on interference against DENV and t ...[more]

PMID: 27893736

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Project description:BackgroundDengue viruses (DENV) are the causative agents of dengue, the world's most prevalent arthropod-borne disease with around 40% of the world's population at risk of infection annually. Wolbachia pipientis, an obligate intracellular bacterium, is being developed as a biocontrol strategy against dengue because it limits replication of the virus in the mosquito. The Wolbachia strain wMel, which has been introduced into the mosquito vector, Aedes aegypti, has been shown to invade and spread to near fixation in field releases. Standard measures of Wolbachia's efficacy for blocking virus replication focus on the detection and quantification of virus in mosquito tissues. Examining the saliva provides a more accurate measure of transmission potential and can reveal the extrinsic incubation period (EIP), that is, the time it takes virus to arrive in the saliva following the consumption of DENV viremic blood. EIP is a key determinant of a mosquito's ability to transmit DENVs, as the earlier the virus appears in the saliva the more opportunities the mosquito will have to infect humans on subsequent bites.Methodology/principal findingsWe used a non-destructive assay to repeatedly quantify DENV in saliva from wMel-infected and Wolbachia-free wild-type control mosquitoes following the consumption of a DENV-infected blood meal. We show that wMel lengthens the EIP, reduces the frequency at which the virus is expectorated and decreases the dengue copy number in mosquito saliva as compared to wild-type mosquitoes. These observations can at least be partially explained by an overall reduction in saliva produced by wMel mosquitoes. More generally, we found that the concentration of DENV in a blood meal is a determinant of the length of EIP, saliva virus titer and mosquito survival.Conclusions/significanceThe saliva-based traits reported here offer more disease-relevant measures of Wolbachia's effects on the vector and the virus. The lengthening of EIP highlights another means, in addition to the reduction of infection frequencies and DENV titers in mosquitoes, by which Wolbachia should operate to reduce DENV transmission in the field.

Project description:Wolbachia bacteria are now being introduced into Aedes aegypti mosquito populations for dengue control. When Wolbachia infections are at a high frequency, they influence the local transmission of dengue by direct virus blocking as well as deleterious effects on vector mosquito populations. However, the effectiveness of this strategy could be influenced by environmental temperatures that decrease Wolbachia density, thereby reducing the ability of Wolbachia to invade and persist in the population and block viruses. We reared wMel-infected Ae. aegypti larvae in the field during the wet season in Cairns, North Queensland. Containers placed in the shade produced mosquitoes with a high Wolbachia density and little impact on cytoplasmic incompatibility. However, in 50% shade where temperatures reached 39°C during the day, wMel-infected males partially lost their ability to induce cytoplasmic incompatibility and females had greatly reduced egg hatch when crossed to infected males. In a second experiment under somewhat hotter conditions (>40°C in 50% shade), field-reared wMel-infected females had their egg hatch reduced to 25% when crossed to field-reared wMel-infected males. Wolbachia density was reduced in 50% shade for both sexes in both experiments, with some mosquitoes cleared of their Wolbachia infections entirely. To investigate the critical temperature range for the loss of Wolbachia infections, we held Ae. aegypti eggs in thermocyclers for one week at a range of cyclical temperatures. Adult wMel density declined when eggs were held at 26-36°C or above with complete loss at 30-40°C, while the density of wAlbB remained high until temperatures were lethal. These findings suggest that high temperature effects on Wolbachia are potentially substantial when breeding containers are exposed to partial sunlight but not shade. Heat stress could reduce the ability of Wolbachia infections to invade mosquito populations in some locations and may compromise the ability of Wolbachia to block virus transmission in the field. Temperature effects may also have an ecological impact on mosquito populations given that a proportion of the population becomes self-incompatible.

Dataset Information

Diet-Induced Nutritional Stress and Pathogen Interference in Wolbachia-Infected Aedes aegypti.

Publications

Diet-Induced Nutritional Stress and Pathogen Interference in Wolbachia-Infected Aedes aegypti.

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