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

Tim W R Möhlmann,Leo Van Overbeek,Constantianus J M Koenraadt,Sven Warris,Els H Nijhuis,Barbara S Drolet,Chantal B F Vogels,Dennis E Te Beest,Gorben P Pijlman,Giel P Göertz,Cajo J F Ter Braak,Marc Hendriks

doi:10.1007/s00248-020-01517-6

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.

Highlights

Symbiotic microorganisms play a key role in the physiology of their insect hosts [1, 2]
To gain insight in the effect of the antibiotic treatment on the composition of gut bacterial communities, the identities of gut bacteria populations in adult female C. nubeculosus, C. sonorensis, and Ae. aegypti were determined by highthroughput 16S rRNA gene sequencing before blood-feeding
To uncover the role that specific gut bacteria may play in virus infection, bacterial species that were significantly different between untreated and antibiotic-treated females were determined by Redundancy analyses (RDA)

Summary

Introduction

Symbiotic microorganisms play a key role in the physiology of their insect hosts [1, 2]. Microorganisms that reside in the insect gut provide extra nutrients to insects with a poor diet, such as aphids and termites [3, 4]. Gut bacteria are important in insect development and fitness. Developmental time was delayed and egg production was.

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