Update on the intricate tango between tick microbiomes and tick‐borne pathogens

Bonnet, Sarah; Pollet, Thomas V.

doi:10.1111/pim.12813

Cited by 71 publications

(82 citation statements)

References 140 publications

(308 reference statements)

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“…Ticks, like many multicellular eukaryotes, harbor a very diverse group of commensal, symbiotic, and pathogenic microorganisms that collectively comprise the microbiome (1,2). This complex microbial system and the tick have evolved an intimate relationship relevant for tick development, nutritional adaptation, reproductive fitness, ecological plasticity, and immunity (3)(4)(5)(6).…”

Section: Introductionmentioning

confidence: 99%

“…Mounting evidence shows that non-pathogenic midgut bacteria may also affect tick vector competence and susceptibility to pathogens transmitted by ticks (7)(8)(9)(10). The development of highthroughput sequencing technologies and bioinformatics tools in the last decade has significantly improved our knowledge of the phylogenetic and genetic diversity, dynamics, and ecology of the microbial communities in several tick species (2). However, the vast majority of studies are restricted to the analysis of the taxonomic composition of the tick microbiome and except for few of them (11)(12)(13)(14), the functional significance of bacterial community structure and diversity remains largely unexplored.…”

Section: Introductionmentioning

confidence: 99%

“…Recent functional metagenomics studies have shown that exploring the taxonomic composition and variability of the tick microbiome underestimates the multidimensional nature of the tick hologenome and that analysis solely based on taxonomic profiles has limited biological significance (11)(12)(13)(14). 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.…”

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: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

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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“…Relatively recent advances in defining tick microbiomes are yielding multiple new insights into tick physiology, reproduction, production of essential molecules not synthesized by the tick, tick-borne pathogen-vector interactions, and a potential new avenue for development of anti-tick vaccines [ 219 , 220 , 221 , 222 , 223 ]. Metagenomic analyses revealed considerable complexity of bacterial genera in life cycle stages and geographical variations in bacterial community structure that indicates a role for environmental influences [ 224 , 225 ].…”

Section: Anti-tick Vaccination Strategiesmentioning

confidence: 99%

Resistance to Ticks and the Path to Anti-Tick and Transmission Blocking Vaccines

Oosterwijk

Wikel

2021

Vaccines

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The medical and veterinary public health importance of ticks and tick-borne pathogens is increasing due to the expansion of the geographic ranges of both ticks and pathogens, increasing tick populations, growing incidence of tick-borne diseases, emerging tick transmitted pathogens, and continued challenges of achieving effective and sustained tick control. The past decades show an increasing interest in the immune-mediated control of tick infestations and pathogen transmission through the use of vaccines. Bovine tick resistance induced by repeated infestations was reported over a century ago. This review addresses the phenomena and immunological underpinning of resistance to tick infestation by livestock and laboratory animals; the scope of tick countermeasures to host immune defenses; and the impact of genomics, functional genomics, and proteomics on dissecting complex tick–host–pathogen interactions. From early studies utilizing tick tissue extracts to salivary gland derived molecules and components of physiologically important pathways in tick gut and other tissues, an increased understanding of these relationships, over time, impacted the evolution of anti-tick vaccine antigen selection. Novel antigens continue to emerge, including increased interest in the tick microbiome. Anti-tick and transmission blocking vaccines targeting pathogen reservoirs have the potential to disrupt enzootic cycles and reduce human, companion, domestic animal, and wildlife exposure to infected ticks.

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“…There is accumulating evidence that non-pathogenic midgut bacteria may also affect tick vector competence and susceptibility to pathogens transmitted by ticks (7-10). The development of high-throughput sequencing technologies and bioinformatics tools in the last decade has significantly improved our knowledge of the phylogenetic and genetic diversity, dynamics, and ecology of the microbial communities in several tick species (2). However, the vast majority of studies of the tick microbiome are restricted to the taxonomic composition, while the functional significance of bacterial community structure and diversity remains largely unexplored (11).…”

Section: Introductionmentioning

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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Update on the intricate tango between tick microbiomes and tick‐borne pathogens

Cited by 71 publications

References 140 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

Resistance to Ticks and the Path to Anti-Tick and Transmission Blocking Vaccines

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

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