A Capsule-Based Model for Immature Hard Tick Stages Infestation on Laboratory Mice

Mateos-Hernández, Lourdes; Rakotobé, Sabine; Defaye, Baptiste; Cabezas-Cruz, Alejandro; Šimo, Ladislav

doi:10.3791/61430

Cited by 12 publications

(15 citation statements)

References 2 publications

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“…Unfed I. ricinus nymphs were obtained from the colonies of UMR-BIPAR, Maisons-Alfort, France. We used previously validated protocol for I. ricinus nymphal stages feeding on mouse ( 17 ). Briefly, the mice were anesthetized by isoflurane and the 2 cm outer diameter EVA-foam capsule (Cosplay Shop, Brugge, Belgium) was glued on their shaved backs using a non-irritating latex glue (Tear Mender, USA).…”

Section: Methodsmentioning

confidence: 99%

“…Microbial co-occurrence networks represent a useful approach to measure the keystoneness of taxa and infer potential interactions between nodes of the functional networks (15,16). In a recent study, Mateos-Hernańdez et al (15,17) introduced anti-tick microbiota vaccines as a tool to target tick microbiota bacteria. The bacterial family Enterobacteriaceae was identified as a keystone taxon in the microbiome of Ixodes ricinus and Ixodes scapularis.…”

Section: Introductionmentioning

confidence: 99%

“…In a recent study, Mateos-Hernández et al. ( 15 , 17 ) introduced anti-tick microbiota vaccines as a tool to target tick microbiota bacteria. The bacterial family Enterobacteriaceae was identified as a keystone taxon in the microbiome of Ixodes ricinus and Ixodes scapularis .…”

Section: Introductionmentioning

confidence: 99%

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Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner

et al. 2021

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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.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner

et al. 2021

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“…The ticks were obtained from the colonies of UMR-BIPAR, Maisons-Alfort, France. Ticks were fed on experimental mice within the EVA-foam (Cosplay Shop, Brugge, Belgium) capsule glued to the animal backs [ 78 ]. Engorged nymphs were kept in a polypropylene tube and maintained with a light-dark (12 h/12 h) cycle in a glass desiccator with >97% relative humidity at 22 °C.…”

Section: Tick Infestationmentioning

confidence: 99%

Anti-Tick Microbiota Vaccine Impacts Ixodes ricinus Performance during Feeding

Mateos-Hernández

Obregón

Mayé³

et al. 2020

Vaccines

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118

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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 α-1,3-galactosyltransferase-deficient-C57BL/6 (α1,3GT KO) mice with a live vaccine containing the Enterobacteriaceae bacterium Escherichia coli strain BL21 revealed that the production of anti-E. coli and anti-α-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 α-1,3-galactosyltransferase genes, and possibly α-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.

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“…Each mouse was infested with twenty I. ricinus nymphs on study day 40. Ticks were placed within EVA-foam (Cosplay Shop, Brugge, Belgium) capsules glued on the back of the animals as previously described (17). Unfed and fully-engorged nymphs were used for DNA extraction.…”

Section: Methodsmentioning

confidence: 99%

Anti-microbiota vaccines modulate the tick microbiome in a taxon-specific manner

Mateos-Hernández

Obregón²,

Wu-Chuang

et al. 2021

Preprint

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Anti-tick microbiota vaccines have been shown to impact tick feeding but its specificity has not been demonstrated. In this study we aimed to investigate the impact of immune targeting of keystone microbiota bacteria on tick performance, and tick microbiota structure and function. Vaccination against Escherichia coli, the selected keystone taxon, increased tick engorgement weight and reduced bacterial diversity in Ixodes ricinus ticks compared to those that fed on mice immunized against Leuconostoc mesenteroides, a non-keystone taxon or mock-immunized group. The abundance of Escherichia-Shigella, but not Leuconostoc was significantly reduced in ticks fed on E. coli-immunized mice and this reduction was correlated with a significant increase in host antibodies (Abs) of the isotype IgM and IgG specific to E. coli proteins. This negative correlation was not observed between the abundance of Leuconostoc in ticks and anti-L. mesenteroides Abs in mice. We also demonstrated by co-occurrence network analysis, that immunization against the keystone bacterium restructure the hierarchy of the microbial community in ticks and that anti-tick microbiota vaccines reduced the resistance of networks to directed removal of taxa. Functional pathways analysis showed that immunization with a live bacterial vaccine can also induce taxon-specific changes in the abundance of pathways. Our results demonstrated that anti-tick microbiota vaccines can modulate the tick microbiome and that the modification is specific to the taxon chosen for host immunization. These results guide interventions for the control of tick infestations and pathogen infection/transmission.

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A Capsule-Based Model for Immature Hard Tick Stages Infestation on Laboratory Mice

Cited by 12 publications

References 2 publications

Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner

Anti-Microbiota Vaccines Modulate the Tick Microbiome in a Taxon-Specific Manner

Anti-Tick Microbiota Vaccine Impacts Ixodes ricinus Performance during Feeding

Anti-microbiota vaccines modulate the tick microbiome in a taxon-specific manner

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