Impact of gut bacteria on the infection and transmission of pathogenic arboviruses by biting midges and mosquitoes

Authors: MOHLMANN, TIM - Wageningen University; VOGELS, CHANTAL - Wageningen University; GOERTZ, GIEL - Wageningen University; PIJLMAN, GORBEN - Wageningen University; TER BRAAK, CAJO - Wageningen University; TE BEEST, DENNIS - Wageningen University; HENDRIKS, MARC - Wageningen University; NIJHUIS, ELS - Wageningen University; WARRIS, SVEN - Wageningen University; Drolet, Barbara; VAN OVERBEEK, LEO - Wageningen University; KOENRAADT, CONSTANTIANUS - Wageningen University

Submitted to: Microbial Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/23/2020
Publication Date: 5/27/2020
Citation: Mohlmann, T., Vogels, C., Goertz, G., Pijlman, G., Ter Braak, C., Te Beest, D., Hendriks, M., Nijhuis, E., Warris, S., Drolet, B.S., Van Overbeek, L., Koenraadt, C. 2020. Impact of gut bacteria on the infection and transmission of pathogenic arboviruses by biting midges and mosquitoes. Microbial Ecology. 80:703-717. https://doi.org/10.1007/s00248-020-01517-6.
DOI: https://doi.org/10.1007/s00248-020-01517-6

Interpretive Summary: The interactions between an insect's gut bacteria and the virus it carries may determine the efficiency with which an insect can transmit that virus during blood feeding on an animal. Here, we investigated the impact of gut bacteria on the infection rate of Schmallenberg virus in two biting midge species, and the infection rate of Zika and Chikungunya viruses in Aedes aegypti mosquitoes. Gut bacteria were manipulated by treating the adult insects with antibiotics. Antibiotic treatment led to changes in gut bacteria for all insects and significantly increased infection rates of midges with Schmallenberg virus. Infection rates of mosquitoes with Zika or Chikungunya virus was not affected. We conclude that in midges, resident gut bacterial populations may normally act to dampen arbovirus transmission and that utilization of antimicrobial compounds at livestock farms might thereby negate this dampening effect and increase transmission of viruses to animals during biting midge blood feeding.

Technical 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 C. sonorensis biting midges for Schmallenberg virus, and of Aedes aegypti mosquitoes for Zika and chikungunya virus. 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 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 significantly increased infection rates of C. nubeculosus with Schmallenberg virus. For C. sonorensis a similar increasing trend of infection rate was observed, whereas 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.