| Summary: | <i>Ixodes scapularis</i> 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. <i>Anaplasma phagocytophilum</i> induces ticks to express <i>I. scapularis</i> antifreeze glycoprotein (IAFGP), a protein with antimicrobial activity, while <i>Borrelia burgdorferi</i> induces the expression of PIXR. Here, we tested the resistance of <i>I. scapularis</i> microbiome to <i>A. phagocytophilum</i> infection, antimicrobial peptide IAFGP, and anti-tick immunity specific to PIXR. We demonstrate that <i>A. phagocytophilum</i> 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 <i>A. phagocytophilum</i> 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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