Impact of Gut Bacteria on the Infection and Transmission of Pathogenic Arboviruses by Biting Midges and Mosquitoes

Abstract

Tripartite interactions among insect vectors, midgut bacteria, and viruses may determine the ability of insects to transmit pathogenic arboviruses. Here, we investigated the impact of gut bacteria on the susceptibility of Culicoides nubeculosus and Culicoides sonorensis biting midges for Schmallenberg virus, and of Aedes aegypti mosquitoes for Zika and chikungunya viruses. Gut bacteria were manipulated by treating the adult insects with antibiotics. The gut bacterial communities were investigated using Illumina MiSeq sequencing of 16S rRNA, and susceptibility to arbovirus infection was tested by feeding insects with an infectious blood meal. Antibiotic treatment led to changes in gut bacteria for all insects. Interestingly, the gut bacterial composition of untreated Ae. aegypti and C. nubeculosus showed Asaia as the dominant genus, which was drastically reduced after antibiotic treatment. Furthermore, antibiotic treatment resulted in relatively more Delftia bacteria in both biting midge species, but not in mosquitoes. Antibiotic treatment and subsequent changes in gut bacterial communities were associated with a significant, 1.8-fold increased infection rate of C. nubeculosus with Schmallenberg virus, but not for C. sonorensis. We did not find any changes in infection rates for Ae. aegypti mosquitoes with Zika or chikungunya virus. We conclude that resident gut bacteria may dampen arbovirus transmission in biting midges, but not so in mosquitoes. Use of antimicrobial compounds at livestock farms might therefore have an unexpected contradictory effect on the health of animals, by increasing the transmission of viral pathogens by biting midges.

The microbiome and mosquito vectorial capacity: rich potential for discovery and translation

“…In addition, microbiota can potentially have other functions in pathogen transmission, since it may be transmitted to the mammalian host during feeding on the host [39]. The role of the gut microbiome in modulating vector competence for several pathogens has been well studied and reviewed extensively in mosquitoes [40][41][42][43][44][45][46][47] and other arthropod vectors [48][49][50][51][52][53][54], so we have focused our attention on the other components of the vectorial capacity equation.…”

Larval Diet Abundance Influences Size and Composition of the Midgut Microbiota of Aedes aegypti Mosquitoes

“…The mosquito midgut microbiota has been shown to influence factors relevant to vector-borne disease transmission (Minard et al, 2013;van Tol and Dimopoulos, 2016;Guégan et al, 2018) including larval development (Coon et al, 2014(Coon et al, , 2017Correa et al, 2018), susceptibility to arboviral infection (Xi et al, 2008;Apte-Deshpande et al, 2012Ramirez et al, 2012Ramirez et al, , 2014Wu et al, 2019;Möhlmann et al, 2020), blood digestion (Gaio et al, 2011), egg production (Gaio et al, 2011;Gendrin et al, 2015), and longevity (Bahia et al, 2014;Ramirez et al, 2014;Gendrin et al, 2015Gendrin et al, , 2016. These observations have led to growing interest in manipulation of the midgut microbiota for vector control and/or prevention of disease transmission.…”

Critical realism as a continuing resource for biological research: the illustrative case study of biting midges and their symbiotic bacteria

“…As BTV replicates in the fat body before travelling to the salivary glands, this indicated to me that possible interactions (like those observed in Wolbachia and mosquitoes) could be occurring in midges in Rickettsia. A study occurring at the same time (Möhlmann et al 2020) described Rickettsia infection of C. sonorensis, a vector species of North America, which is already colonized and is used as a gold standard for infection experiments. Thus, by the end of the funded project a model species to test Rickettsiaeffects on midge-borne viruses was available and I could complete and submit my PhD thesis.…”