Abstract
BackgroundWolbachia pipientis is a common endosymbiotic bacterium of arthropods that strongly inhibits dengue virus (DENV) infection and transmission in the primary vector, the mosquito Aedes aegypti. For that reason, Wolbachia-infected Ae. aegypti are currently being released into the field as part of a novel strategy to reduce DENV transmission. However, there is evidence that DENV can be transmitted vertically from mother to progeny, and this may help the virus persist in nature in the absence of regular human transmission. The effect of Wolbachia infection on this process had not previously been examined.ResultsWe challenged Ae. aegypti with different Brazilian DENV isolates either by oral feeding or intrathoracic injection to ensure disseminated infection. We examined the effect of Wolbachia infection on the prevalence of DENV infection, and viral load in the ovaries. For orally infected mosquitoes, Wolbachia decreased the prevalence of infection by 71.29%, but there was no such effect when the virus was injected. Interestingly, regardless of the method of infection, Wolbachia infection strongly reduced DENV load in the ovaries. We then looked at the effect of Wolbachia on vertical transmission, where we observed only very low rates of vertical transmission. There was a trend towards lower rates in the presence of Wolbachia, with overall maximum likelihood estimate of infection rates of 5.04 per 1000 larvae for mosquitoes without Wolbachia, and 1.93 per 1000 larvae for Wolbachia-infected mosquitoes, after DENV injection. However, this effect was not statistically significant.ConclusionsOur data support the idea that vertical transmission of DENV is rare in nature, even in the absence of Wolbachia. Indeed, we observed that vertical transmission rates were low even when the midgut barrier was bypassed, which might help to explain why we only observed a trend towards lower vertical transmission rates in the presence of Wolbachia. Nevertheless, the low prevalence of disseminated DENV infection and lower DENV load in the ovaries supports the hypothesis that the presence of Wolbachia in Ae. aegypti would have an effect on the vertical transmission of DENV in the field.
Highlights
Wolbachia pipientis is a common endosymbiotic bacterium of arthropods that strongly inhibits dengue virus (DENV) infection and transmission in the primary vector, the mosquito Aedes aegypti
In ovaries dissected from -Aedes aegypti uninfected by Wolbachia (Wolb) and +Wolb mosquitoes that were orally challenged with Dengue virus serotypes 1 (DENV-4), we observed 71.29% decrease in prevalence of infection associated with wMel (Fig. 1, Fisher’s exact test: P = 0.0002, OR = 0.0875, CI = 0.0237–0.327), which could indicate that the anti-DENV effect of Wolbachia can operate on the tissue level, or that the general inhibitory effect of Wolbachia limits the amount of virus that reaches the ovaries [21]
Regardless of the method of viral challenge, we observed that significantly decreased DENV load in the ovaries was associated with the presence of wMel (Mann-Whitney U-tests: DENV-4 oral infection: U = 4, n1 = 16, n2 = 7, P < 0.0001; DENV-1 injection: U = 116, n1 = 20, n2 = 19, P = 0.0379; DENV-4 injection: U = 112, n1 = 19, n2 = 21, P = 0.0173)
Summary
Wolbachia pipientis is a common endosymbiotic bacterium of arthropods that strongly inhibits dengue virus (DENV) infection and transmission in the primary vector, the mosquito Aedes aegypti. WMel infection greatly decreases viral prevalence in the salivary glands and more importantly the saliva, and likely reduces vector competence for DENV [3,4,5] This anti-DENV effect forms the basis of the Wolbachia transmission blocking approach, which is currently being used around the world to reduce the DENV burden (www.eliminatedengue.com). In this strategy, wMel-infected mosquitoes are released into the field, where the bacterium can spread to high levels in wild populations due to cytoplasmic incompatibility, a type of reproductive incompatibility that favours the propagation of Wolbachia-infected mosquitoes and acts as a form of drive [6]. The widespread deployment of wMel-infected mosquitoes in disease-endemic areas could potentially lead to a reduction in the transmission of DENV, or other viruses such as Zika and chikungunya [7,8,9,10]
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