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

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 ex...

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Autores principales: Estrada-Peña, Agustín, Cabezas-Cruz, Alejandro, Obregón, Dasiel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7238099/
https://www.ncbi.nlm.nih.gov/pubmed/32331444
http://dx.doi.org/10.3390/pathogens9040309
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author Estrada-Peña, Agustín
Cabezas-Cruz, Alejandro
Obregón, Dasiel
author_facet Estrada-Peña, Agustín
Cabezas-Cruz, Alejandro
Obregón, Dasiel
author_sort Estrada-Peña, Agustín
collection PubMed
description 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.
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spelling pubmed-72380992020-05-28 Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides Estrada-Peña, Agustín Cabezas-Cruz, Alejandro Obregón, Dasiel Pathogens Article 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. MDPI 2020-04-22 /pmc/articles/PMC7238099/ /pubmed/32331444 http://dx.doi.org/10.3390/pathogens9040309 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Estrada-Peña, Agustín
Cabezas-Cruz, Alejandro
Obregón, Dasiel
Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides
title Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides
title_full Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides
title_fullStr Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides
title_full_unstemmed Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides
title_short Resistance of Tick Gut Microbiome to Anti-Tick Vaccines, Pathogen Infection and Antimicrobial Peptides
title_sort resistance of tick gut microbiome to anti-tick vaccines, pathogen infection and antimicrobial peptides
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7238099/
https://www.ncbi.nlm.nih.gov/pubmed/32331444
http://dx.doi.org/10.3390/pathogens9040309
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