Abstract
The lack of tools for the precise manipulation of the tick microbiome is currently a major limitation to achieve mechanistic insights into the tick microbiome. Anti-tick microbiota vaccines targeting keystone bacteria of the tick microbiota alter tick feeding, but their impact on the taxonomic and functional profiles of the tick microbiome has not been tested. In this study, we immunized a vertebrate host model (Mus musculus) with live bacteria vaccines targeting keystone (i.e., Escherichia-Shigella) or non-keystone (i.e., Leuconostoc) taxa of tick microbiota and tested the impact of bacterial-specific antibodies (Abs) on the structure and function of tick microbiota. We also investigated the effect of these anti-microbiota vaccines on mice gut microbiota composition. Our results showed that the tick microbiota of ticks fed on Escherichia coli-immunized mice had reduced Escherichia-Shigella abundance and lower species diversity compared to ticks fed on control mice immunized with a mock vaccine. Immunization against keystone bacteria restructured the hierarchy of nodes in co-occurrence networks and reduced the resistance of the bacterial network to taxa removal. High levels of E. coli-specific IgM and IgG were negatively correlated with the abundance of Escherichia-Shigella in tick microbiota. These effects were not observed when Leuconostoc was targeted with vaccination against Leuconostoc mesenteroides. Prediction of functional pathways in the tick microbiome using PICRUSt2 revealed that E. coli vaccination reduced the abundance of lysine degradation pathway in tick microbiome, a result validated by qPCR. In contrast, the gut microbiome of immunized mice showed no significant alterations in the diversity, composition and abundance of bacterial taxa. Our results demonstrated that anti-tick microbiota vaccines are a safe, specific and an easy-to-use tool for manipulation of vector microbiome. These results guide interventions for the control of tick infestations and pathogen infection/transmission.
Highlights
Ticks, like many multicellular eukaryotes, harbor a very diverse group of commensal, symbiotic, and pathogenic microorganisms that collectively comprise the microbiome [1, 2]
Immunization with the Enterobacteriaceae bacterium Escherichia coli elicited an anti-E. coli IgM and IgG antibody (Ab) response associated with increased engorgement weight of I. ricinus nymphs that fed on C57BL/6 mice and high mortality in ticks that fed on a-1,3-galactosyltransferase (a1,3GT)deficient C57BL/6 mice compared with the ticks that fed on the control group
The results suggest that host Abs bind and kill EscherichiaShigella bacteria in the tick microbiome, a conclusion supported by two evidences: (i) a negative correlation between the levels of both anti-E. coli IgM and IgG and the relative abundance of Escherichia-Shigella in the tick microbiome and (ii) the binding of anti-E. coli IgM and IgG to E. coli ex vivo
Summary
Like many multicellular eukaryotes, harbor a very diverse group of commensal, symbiotic, and pathogenic microorganisms that collectively comprise the microbiome [1, 2]. The native tick microbiome is likely composed of bacteria, archaea, fungi, protozoans and viruses with diverse functional capacities, which are engaged in a complex network of cooperative and competitive interactions [1, 2]. Some of these microorganisms, known as keystone species, co-occur with many others and may have a large regulatory effect on the structure, organization, and function of the tick microbiome. The functional capacity of the tick microbiome is not equal to the overall number of its individual components, as microbial species strongly and frequently interact with one another and form a complex functional network [13, 14], which can be considered as a fundamental unit in microbial communities of ticks
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