Species identity, life history, and geographic distance influence gut bacterial communities in lab-reared and European field-collected Culicoides biting midges

Authors: MOHLMANN, TIM - 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: 7/14/2021
Publication Date: 8/26/2021
Citation: Mohlmann, T.W., Ter Braak, C.J., Te Beest, D., Hendriks, M., Nijhuis, E.H., Warris, S., Drolet, B.S., Van Overbeek, L., Koenraadt, C.J. 2021. Species identity, life history, and geographic distance influence gut bacterial communities in lab-reared and European field-collected Culicoides biting midges. Microbial Ecology. 84, pages267–284 (2022). https://doi.org/10.1007/s00248-021-01822-8.
DOI: https://doi.org/10.1007/s00248-021-01822-8

Interpretive Summary: Insects are exposed to bacteria in the environment during their development. Thus, bacteria are part of the insect's midgut and can influence many physiological traits. Gut bacteria may even reduce or block the transmission of arboviruses. Culicoides biting midges are important arboviral vectors of several livestock and wildlife diseases. Understanding what bacterial communities are in midge midguts informs how they can be manipulated and ultimately used as novel tools to control pathogen transmission. Our results show that metamorphosis is not only a key event in the development of the biting midge itself, but also for its midgut bacterial community composition, which changed significantly after pupation. Differences seen in bacterial communities among different species and habitats/countries might partly explain the observed inter- and intra-species variability in vector competence of biting midges.

Technical Abstract: Bacteria are part of the insect gut system and influence many physiological traits of their host. Gut bacteria may even reduce or block the transmission of arboviruses in several species of arthropod vectors. Culicoides biting midges are important arboviral vectors of several livestock and wildlife diseases, yet limited information is available on their gut bacterial communities. Addressing this gap will help inform how these communities can be manipulated and ultimately used as novel tools to control pathogens. To assess how bacterial communities change during the life stages of lab-reared C. nubeculosus and C. sonorensis, endosymbiotic bacteria were identified using Illumina sequencing of 16S rRNA and taxonomically characterized. Analyses were conducted to determine how gut bacterial communities in adults are influenced by species identity and geographic distance among biting midge populations. Communities of the two lab-reared Culicoides species significantly changed after pupation and with maturation into six-day-old adults. Pseudomonas, Burkholderiaceae and Leucobacter bacteria were part of a core community that was trans-stadially transmitted and found throughout their life cycle. Among field-collected biting midges, the bacterial communities were unique for almost each species. Cardinium, Rickettsia and Wolbachia were some of the most abundant bacteria in midges collected from wetlands. Only Pseudomonas was present in high relative abundance in all field-collected species. In this study, species identity, as well as geographic distance, influenced the gut bacterial communities and may partly explain known inter- and intra-species variability in vector competence. Additionally, stably associated bacterial species could be candidates for paratransgenic strategies to control vector-borne pathogens.