Dataset Information

Anti-Tick Microbiota Vaccine Impacts Ixodes ricinus Performance during Feeding.

ABSTRACT: The tick microbiota is a highly complex ensemble of interacting microorganisms. Keystone taxa, with a central role in the microbial networks, support the stability and fitness of the microbial communities. The keystoneness of taxa in the tick microbiota can be inferred from microbial co-occurrence networks. Microbes with high centrality indexes are highly connected with other taxa of the microbiota and are expected to provide important resources to the microbial community and/or the tick. We reasoned that disturbance of vector microbiota by removal of ubiquitous and abundant keystone bacteria may disrupt the tick-microbiota homeostasis causing harm to the tick host. These observations and reasoning prompted us to test the hypothesis that antibodies targeting keystone bacteria may harm the ticks during feeding on immunized hosts. To this aim, in silico analyses were conducted to identify keystone bacteria in the microbiota of Ixodes nymphs. The family Enterobacteriaceae was among the top keystone taxa identified in Ixodes microbiota. Immunization of ?-1,3-galactosyltransferase-deficient-C57BL/6 (?1,3GT KO) mice with a live vaccine containing the Enterobacteriaceae bacterium Escherichia coli strain BL21 revealed that the production of anti-E. coli and anti-?-Gal IgM and IgG was associated with high mortality of I. ricinus nymphs during feeding. However, this effect was absent in two different strains of wild type mice, BALB/c and C57BL/6. This result concurred with a wide distribution of ?-1,3-galactosyltransferase genes, and possibly ?-Gal, in Enterobacteriaceae and other bacteria of tick microbiota. Interestingly, the weight of I. ricinus nymphs that fed on E. coli-immunized C57BL/6 was significantly higher than the weight of ticks that fed on C57BL/6 immunized with a mock vaccine. Our results suggest that anti-tick microbiota vaccines are a promising tool for the experimental manipulation of vector microbiota, and potentially the control of ticks and tick-borne pathogens.

SUBMITTER: Mateos-Hernandez L

PROVIDER: S-EPMC7711837 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Anti-Tick Microbiota Vaccine Impacts <i>Ixodes ricinus</i> Performance during Feeding.

Mateos-Hernández Lourdes L Obregón Dasiel D Maye Jennifer J Borneres Jeremie J Versille Nicolas N de la Fuente José J Estrada-Peña Agustín A Hodžić Adnan A Šimo Ladislav L Cabezas-Cruz Alejandro A

Vaccines 20201121 4

The tick microbiota is a highly complex ensemble of interacting microorganisms. Keystone taxa, with a central role in the microbial networks, support the stability and fitness of the microbial communities. The keystoneness of taxa in the tick microbiota can be inferred from microbial co-occurrence networks. Microbes with high centrality indexes are highly connected with other taxa of the microbiota and are expected to provide important resources to the microbial community and/or the tick. We rea ...[more]

PMID: 33233316

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Project description:Background:Ticks can survive long periods without feeding but, when feeding, ingest large quantities of blood, resulting in a more than 100-fold increase of body volume. We study morphological adaptations to changes in opisthosoma volume during feeding in the castor bean tick, Ixodes ricinus. We aim to understand the functional morphological features that accommodate enormous changes in volume changes. Methods:Using light and electron microscopy, we compare the cuticle and epidermis of the alloscutum, the epithelium of the midgut diverticula, and the tracheae of adult female ticks when fasting, semi-engorged, and fully engorged. Results:Our results add to an existing body of knowledge that the area of the epidermis increases by cellular differentiation, cellular hypertrophy, and changes in the shape of epithelial cells from pseudostratified to single layered prismatic in semi-engorged ticks, and to thin squamous epithelium in fully engorged ticks. We did not find evidence for cell proliferation. The midgut diverticula accommodate the volume increase by cellular hypertrophy and changes in cell shape. In fully engorged ticks, the epithelial cells of the midgut diverticula are stretched to an extremely thin, squamous epithelium. Changes in size and shape (and cell divisions) contribute to the accommodation of volume changes. Tracheae do not increase in size, but extend in length, thus following the volume changes of the opisthosoma in feeding ticks to secure oxygen supply to the internal organs. Conclusions:Changes of epithelial tissue configuration in the epidermis and the midgut diverticula are described as important components of the morphological response to feeding in ticks. We provide evidence for a previously unknown mechanism hosted in the endocuticle of the tracheae that allows the tracheae of castor bean ticks to expand when the body volume increases and the distance between the respiratory spiracle and the oxygen demanding tissue enlarges. This is the first report of expandable tracheae in arthropods.

Project description:Anti-tick vaccines have the potential to be an environmentally friendly and cost-effective option for tick control. In vaccine development, the identification of efficacious antigens forms the major bottleneck. In this study, the efficacy of immunization with recombinant ferritin 2 and native tick protein extracts (TPEs) against Ixodes ricinus infestations in calves was assessed in two immunization experiments. In the first experiment, each calf (n = 3) was immunized twice with recombinant ferritin 2 from I. ricinus (IrFER2), TPE consisting of soluble proteins from the internal organs of partially fed I. ricinus females, or adjuvant, respectively. In the second experiment, each calf (n = 4) was immunized with protein extracts from the midgut (ME) of partially fed females, the salivary glands (SGE) of partially fed females, a combination of ME and SGE, or adjuvant, respectively. Two weeks after the booster immunization, calves were challenged with 100 females and 200 nymphs. Blood was collected from the calves before the first and after the second immunization and fed to I. ricinus females and nymphs using an in vitro artificial tick feeding system. The two calves vaccinated with whole TPE and midgut extract (ME) showed hyperemia on tick bite sites 2 days post tick infestation and exudative blisters were observed in the ME-vaccinated animal, signs that were suggestive of a delayed type hypersensitivity (DTH) reaction. Significantly fewer ticks successfully fed on the three animals vaccinated with TPE, SGE, or ME. Adults fed on the TPE and ME vaccinated animals weighed significantly less. Tick feeding on the IrFER2 vaccinated calf was not impaired. The in vitro feeding of serum or fresh whole blood collected from the vaccinated animals did not significantly affect tick feeding success. Immunization with native I. ricinus TPEs thus conferred a strong immune response in calves and significantly reduced the feeding success of both nymphs and adults. In vitro feeding of serum or blood collected from vaccinated animals to ticks did not affect tick feeding, indicating that antibodies alone were not responsible for the observed vaccine immunity.

Project description:Ticks, pathogens, and vertebrates interact in a background of environmental features that regulate the densities of ticks and vertebrates, affecting their contact rates and thence the circulation of the pathogens. Regional scale studies are invaluable sources of information about the regulation of these interactions, but a large-scale analysis of the interaction of communities of ticks, hosts, and the environment has been never modeled. This study builds on network analysis, satellite-derived climate and vegetation, and environmental modeling, quantifying the interactions between the tick Ixodes ricinus and the transmitted bacteria of the complex Borrelia burgdorferi s.l. in the Western Palaearctic. We derived the rates of contact of the tick with 162 species of vertebrates recorded as hosts, and the relative importance of each vertebrate in the circulation of the pathogen. We compiled more than 11 millions of pairs of coordinates of the vertebrates, deriving distribution models of each species and the relative faunal composition in the target territory. The results of the modeling of the distribution of the tick and its hosts, weighted by their importance in the circulation of Borrelia captured the spatial patterns of interactions that allow the circulation of the pathogen. Results indicate that both I. ricinus and B. burgdorferi s.l. are supported in the Western Palaearctic by complex communities of vertebrates, which have large distribution ranges. This high functional redundancy results in the pervasiveness of B. burgdorferi s.l., which depends on the gradient of contributions of the large community of vertebrates, instead of relying on a few dominant vertebrates, which was the prevailing paradigm. Most prominent reservoirs of the pathogen are distributed in specific regions of the environmental niche. However, literally dozens of potential reservoirs can colonize many other environmental regions, marginally but efficiently contributing to the circulation of the pathogen. These results consistently point to the need of evaluating the beta-diversity of the community of vertebrates acting as reservoirs of the pathogen to better know the interactions with the vector. They also demonstrate why the pathogen is so resilient to perturbations in the composition of the reservoirs.

Dataset Information

Anti-Tick Microbiota Vaccine Impacts Ixodes ricinus Performance during Feeding.

Publications

Anti-Tick Microbiota Vaccine Impacts <i>Ixodes ricinus</i> Performance during Feeding.

Similar Datasets

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