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

Lourdes Mateos-Hernández,Nicolas Versille,Jennifer Maye,Jeremie Borneres,Adnan Hodžić,José De La Fuente,Dasiel Obregón,Ladislav Šimo,Alejandro Cabezas-Cruz,Agustín Estrada-Peña

doi:10.3390/vaccines8040702

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 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.

Highlights

IntroductionNon-pathogenic microbes associated with ticks impact vector physiology and survival [1]
Non-pathogenic microbes associated with ticks impact vector physiology and survival [1].Some endosymbionts, such as Francisella sp., contribute to the synthesis of vitamin B, a nutritional component essential for ticks and absent in the blood meal
Evidence suggests that some bacteria have key roles in the structure, organization and functioning of tick microbiota, since they constitute a reduced taxonomic core of the tick gut microbiota that remains stable despite biological disturbance [5]

Summary

Introduction

Non-pathogenic microbes associated with ticks impact vector physiology and survival [1] Some endosymbionts, such as Francisella sp., contribute to the synthesis of vitamin B, a nutritional component essential for ticks and absent in the blood meal. Vitamin B synthesis genes are not restricted to Francisella [1] or Coxiella [3], but are widely distributed in some genera of tick microbiota [4]. This suggests that nutritional complementation in ticks can be an attribute of symbionts, and of tick microbiota bacteria [4]. Microbial communities harbor keystone taxa which are highly connected and have a great explanatory power of the community structure and functioning irrespective of their abundance [7]

Methods

Discussion

Conclusion