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Open AccessArticle

Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides

by Agustín Estrada-Peña 1,2,*,†, Alejandro Cabezas-Cruz 3,*,† and Dasiel Obregón 4,5,*,†
1
Faculty of Veterinary Medicine, University of Zaragoza, 50013 Zaragoza, Spain
2
Group of Research on Emerging Zoonoses, Instituto Agroalimentario de Aragón (IA2), 50013 Zaragoza, Spain
3
UMR BIPAR, INRAE, ANSES, École Nationale Vétérinaire d’Alfort, Université Paris-Est, 94700 Maisons-Alfort, France
4
Center for Nuclear Energy in Agriculture, University of São Paulo, Piracicaba, São Paulo 13400-970, Brazil
5
School of Environmental Sciences, University of Guelph, Guelph, ON N1G 2W1, Canada
*
Authors to whom correspondence should be addressed.
All authors contributed equally.
Pathogens 2020, 9(4), 309; https://doi.org/10.3390/pathogens9040309
Received: 20 March 2020 / Revised: 16 April 2020 / Accepted: 21 April 2020 / Published: 22 April 2020
(This article belongs to the Special Issue New Frontiers in Tick Research)
Ixodes scapularis ticks harbor microbial communities including pathogenic and non-pathogenic microbes. Pathogen infection increases the expression of several tick gut proteins, which disturb the tick gut microbiota and impact bacterial biofilm formation. Anaplasma phagocytophilum induces ticks to express I. scapularis antifreeze glycoprotein (IAFGP), a protein with antimicrobial activity, while Borrelia burgdorferi induces the expression of PIXR. Here, we tested the resistance of I. scapularis microbiome to A. phagocytophilum infection, antimicrobial peptide IAFGP, and anti-tick immunity specific to PIXR. We demonstrate that A. phagocytophilum infection and IAFGP affect the taxonomic composition and taxa co-occurrence networks, but had limited impact on the functional traits of tick microbiome. In contrast, anti-tick immunity disturbed the taxonomic composition and the functional profile of tick microbiome, by increasing both the taxonomic and pathways diversity. Mechanistically, we show that anti-tick immunity increases the representation and importance of the polysaccharide biosynthesis pathways involved in biofilm formation, while these pathways are under-represented in the microbiome of ticks infected by A. phagocytophilum or exposed to IAFGP. These analyses revealed that tick microbiota is highly sensitive to anti-tick immunity, while it is less sensitive to pathogen infection and antimicrobial peptides. Results suggest that biofilm formation may be a defensive response of tick microbiome to anti-tick immunity. View Full-Text
Keywords: Ixodes scapularis; microbiota; disturbance; functional redundancy; core microbiome Ixodes scapularis; microbiota; disturbance; functional redundancy; core microbiome
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Estrada-Peña, A.; Cabezas-Cruz, A.; Obregón, D. Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides. Pathogens 2020, 9, 309.

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