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A Wolbachia triple-strain infection generates self-incompatibility in Aedes albopictus and transmission instability in Aedes aegypti.

ABSTRACT: Artificially-introduced transinfections of the intracellular bacterium Wolbachia pipientis have the potential to reduce the vectorial capacity of mosquito populations for viruses such as dengue and chikungunya. Aedes albopictus has two native strains of Wolbachia, but their replacement with the non-native wMel strain blocks transmission of both viruses. The pattern of cytoplasmic incompatiiblity generated by wMel with wild-types is bidirectional. Novel-plus-native-strain co-infection is predicted to lead to a more efficient population spread capacity; from a bi-directional to a uni-directional cytoplasmic incompatibility (CI) model.A novel-plus-native-strain triple-infection in Ae. albopictus (wAlbAwAlbBwMel) was generated. Although triple-infected females were fully reproductively viable with uninfected males, they displayed self-incompatibility. qPCR of specific strains in dissected tissues suggested that this may be due to the displacement of one of the native strains (wAlbA) from the ovaries of triple-infected females. When the triple strain infection was transferred into Aedes aegypti it displayed an unexpectedly low level of transmission fidelity of the three strains in this species.These results suggest that combining Wolbachia strains can lead to co-infection interactions that can affect outcomes of CI and maternal transmission.

SUBMITTER: Ant TH

PROVIDER: S-EPMC5948879 | biostudies-other | 2018 May

REPOSITORIES: biostudies-other

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A Wolbachia triple-strain infection generates self-incompatibility in Aedes albopictus and transmission instability in Aedes aegypti.

Ant Thomas H TH Sinkins Steven P SP

Parasites & vectors 20180511 1

<h4>Background</h4>Artificially-introduced transinfections of the intracellular bacterium Wolbachia pipientis have the potential to reduce the vectorial capacity of mosquito populations for viruses such as dengue and chikungunya. Aedes albopictus has two native strains of Wolbachia, but their replacement with the non-native wMel strain blocks transmission of both viruses. The pattern of cytoplasmic incompatiiblity generated by wMel with wild-types is bidirectional. Novel-plus-native-strain co-in ...[more]

PMID: 29751814

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Project description:BackgroundNew approaches to preventing chikungunya virus (CHIKV) are needed because current methods are limited to controlling mosquito populations, and they have not prevented the invasion of this virus into new locales, nor have they been sufficient to control the virus upon arrival. A promising candidate for arbovirus control and prevention relies on the introduction of the intracellular bacterium Wolbachia into Aedes aegypti mosquitoes. This primarily has been proposed as a tool to control dengue virus (DENV) transmission; however, evidence suggests Wolbachia infections confer protection for Ae. aegypti against CHIKV. Although this approach holds much promise for limiting virus transmission, at present our understanding of the ability of CHIKV to infect, disseminate, and be transmitted by wMel-infected Ae. aegypti currently being used at Wolbachia release sites is limited.Methodology/principal findingsUsing Ae. aegypti infected with the wMel strain of Wolbachia that are being released in Medellin, Colombia, we report that these mosquitoes have reduced vector competence for CHIKV, even with extremely high viral titers in the bloodmeal. In addition, we examined the dynamics of CHIKV infection over the course of four to seven days post feeding. Wolbachia-infected mosquitoes remained non-infective over the duration of seven days, i.e., no infectious virus was detected in the saliva when exposed to bloodmeals of moderate viremia, but CHIKV-exposed, wild type mosquitoes did have viral loads in the saliva consistent with what has been reported elsewhere. Finally, the presence of wMel infection had no impact on the lifespan of mosquitoes as compared to wild type mosquitoes following CHIKV infection.Conclusions/significanceThese results could have an impact on vector control strategies in areas where Ae. aegypti are transmitting both DENV and CHIKV; i.e., they argue for further exploration, both in the laboratory and the field, on the feasibility of expanding this technology beyond DENV.

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.

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.

Dataset Information

A Wolbachia triple-strain infection generates self-incompatibility in Aedes albopictus and transmission instability in Aedes aegypti.

Publications

A Wolbachia triple-strain infection generates self-incompatibility in Aedes albopictus and transmission instability in Aedes aegypti.

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