Modulation of the tick gut milieu by a secreted tick protein favors Borrelia burgdorferi colonization

Sukanya Narasimhan (), Tim J. Schuijt, Nabil M. Abraham, Nallakkandi Rajeevan, Jeroen Coumou, Morven Graham, Andrew Robson, Ming-Jie Wu, Sirlei Daffre, Joppe W. Hovius and Erol Fikrig ()
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Sukanya Narasimhan: Yale University School of Medicine
Tim J. Schuijt: University of Amsterdam
Nabil M. Abraham: Yale University School of Medicine
Nallakkandi Rajeevan: Yale Centre for Medical Informatics
Jeroen Coumou: University of Amsterdam
Morven Graham: Yale Centre for Cellular and Molecular Imaging
Andrew Robson: Yale University School of Medicine
Ming-Jie Wu: Yale University School of Medicine
Sirlei Daffre: Universidade de São Paulo
Joppe W. Hovius: University of Amsterdam
Erol Fikrig: Yale University School of Medicine

Nature Communications, 2017, vol. 8, issue 1, 1-17

Abstract: Abstract The Lyme disease agent, Borrelia burgdorferi, colonizes the gut of the tick Ixodes scapularis, which transmits the pathogen to vertebrate hosts including humans. Here we show that B. burgdorferi colonization increases the expression of several tick gut genes including pixr, encoding a secreted gut protein with a Reeler domain. RNA interference-mediated silencing of pixr, or immunity against PIXR in mice, impairs the ability of B. burgdorferi to colonize the tick gut. PIXR inhibits bacterial biofilm formation in vitro and in vivo. Abrogation of PIXR function in vivo results in alterations in the gut microbiome, metabolome and immune responses. These alterations influence the spirochete entering the tick gut in multiple ways. PIXR abrogation also impairs larval molting, indicative of its role in tick biology. This study highlights the role of the tick gut in actively managing its microbiome, and how this impacts B. burgdorferi colonization of its arthropod vector.

Date: 2017
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DOI: 10.1038/s41467-017-00208-0

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