Biotic and abiotic factors shape the microbiota of wild‐caught populations of the arbovirus vectorCulicoides imicola

Abstract

Biting midges of the genus Culicoides are known vectors of arboviruses affecting human and animal health. However, little is known about Culicoides imicola microbiota and its influence on this insect's biology. In this study, the impact of biotic and abiotic factors on C. imicola microbiota was characterized using shotgun-metagenomic sequencing of whole-body DNA samples. Wild-caught C. imicola adult nulliparous females were sampled in two locations from Sicily, Italy. The climatic variables of temperature and soil moisture from both localities were recorded together with potential host bloodmeal sources. Shared core microbiome among C. imicola populations included Pseudomonas, Escherichia, Halomonas, Candidatus Zinderia, Propionibacterium, and Schizosaccharomyces. Specific and unique taxa were also found in C. imicola from each location, highlighting similarities and differences in microbiome composition between the two populations. DNA and protein identification showed differences in host preferences between the two populations, with Homo sapiens and Canis lupus familiaris L. being the preferred bloodmeal source in both locations. A principal component analysis showed that the combined effect of host preferences (H. sapiens) and local soil moisture factors shape the microbiome composition of wild-caught populations of C. imicola. These results contribute to characterizing the role of the microbiome in insect adaptation and its utility in predicting geographic expansion of Culicoides species with potential implications for the control of vector-borne diseases.

Habitat disturbance and the organization of bacterial communities in Neotropical hematophagous arthropods

“…Our results are generally similar to those obtained in previous studies, where arthropod vectors species were dominated by Proteobacteria, including Gammaproteobacteria , Betaproteobacteria , Alphaproteobacteria , and to a lesser extent by Firmicutes, commonly Bacilli and Actinobacteria [13,18,44–46,77,78], These groups included bacterial genera previously described for Culex [13,44,46,77], Culicoides [21,38], Lutzomyia [37,79], Haemaphysalis [78,80] and Amblyomma [42,81].…”

“…Studies regarding the microbiome of disease vectors have attempted to describe the structure and bacterial composition of specific taxonomic groups of arthropods, and to understand how it varies according to particular ecological or physiological factors, with the most comprehensive studies focused on mosquitoes [10] and ticks [2]. Although some studies have considered the impact of habitat or environment type on arthropod microbiota in mosquitoes [11–16], ticks [17–20] and biting midges [21], none to date have investigated the role of habitat disturbance in shaping bacterial assemblages among co-distributed hematophagous arthropods.…”

“…For example, members of Enterobacteriae are correlated with higher Plasmodium infection rates in Anopheles mosquitoes, while Serratia odorifera can increase the replication of both DENV and CHIKV in the midgut of Aedes aegypti [28,36]. Although, studies have endeavored to characterize the core microbiome of members of Psychodidae sand flies, Ceratopogonidae biting midges and Ixodidae hard ticks, it is still generally unknown how similar or different their microbiomes are, and whether some bacteria may influence disease transmission dynamics in these arthropod assemblages [18,19,21,37–42]. Nonetheless, some studies have revealed that resident bacteria are essential for the development of Leishmania parasite in Psychodidae through antibiotic treatment [37,43].…”

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

“…Recently, several studies have shown that bacteria in the gut of laboratory-reared mosquitoes and biting midges are different from those found in field populations [60][61][62][63]. Therefore, our findings may not directly apply to field populations of mosquitoes and biting midges.…”

Important Dispersal Capacity of One Main Species Vector of Bluetongue and Schmallenberg Viruses Culicoides Obsoletus (Diptera: Ceratopogonidae) Revealed by Landscape Genetic Analyses 

“…The altitude therefore does not act as a barrier between sampling sites located at relatively low altitude. It would thus be interesting to integrate in future studies sampling sites with a high altitude above 1,000 m, which is possible for C. obsoletus highlighting a large altitudinal range [91]. However, it is possible that the altitude does not directly impact the dispersal activity of Culicoides, but only the replication or viral infection of BTV due to low temperature.…”