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Borrelia infection in rodent host has dramatic effects on the microbiome of ticks

Phineas T. Hamilton, Elodie Maluenda, Anouk Sarr, Alessandro Belli, Georgia Hurry, Olivier Duron, Olivier Plantard, View ORCID ProfileMaarten J. Voordouw
doi: https://doi.org/10.1101/2021.03.15.435198
Phineas T. Hamilton
1Deeley Research Centre, BC Cancer, Victoria BC, Canada
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  • For correspondence: phin.hamilton@gmail.com maarten.voordouw@usask.ca
Elodie Maluenda
2Laboratory of Ecology and Evolution of Parasites, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
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Anouk Sarr
2Laboratory of Ecology and Evolution of Parasites, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
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Alessandro Belli
3Laboratory of Ecology and Epidemiology of Parasites, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
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Georgia Hurry
4Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Canada
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Olivier Duron
5Centre of Research in Ecology and Evolution of Diseases (CREES), Montpellier, France
6MIVEGEC (Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle), Univ. Montpellier (UM) - Centre National de la Recherche Scientifique (CNRS) - Institut pour la Recherche et le Développement (IRD), Montpellier, France
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Olivier Plantard
7INRAE, Oniris, BIOEPAR, 44300, Nantes, France
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Maarten J. Voordouw
2Laboratory of Ecology and Evolution of Parasites, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
4Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Canada
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  • ORCID record for Maarten J. Voordouw
  • For correspondence: phin.hamilton@gmail.com maarten.voordouw@usask.ca
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Abstract

Background Vector-borne diseases remain major causes of human morbidity and mortality. It is increasingly recognized that the community of microbes inhabiting arthropods can strongly affect their vector competence, but the role of the tick microbiome in Borrelia transmission – the cause of Lyme disease – remains unclear.

Results Here, we use a large-scale experiment to clarify the reciprocal interactions between Borrelia afzelii and the microbiome of Ixodes ricinus, its primary vector. In contrast to other reports, we find that depletion of the bacterial microbiome in larval ticks has no effect on their subsequent acquisition of B. afzelii during blood feeding on infected mice. Rather, exposure to B. afzelii-infected hosts drives pervasive changes to the tick microbiome, decreasing overall bacterial abundance, shifting bacterial community composition, and increasing bacterial diversity. These effects appear to be independent of the acquisition of B. afzelii by ticks, suggesting they are mediated by physiological or immunological aspects of B. afzelii infection in the rodent host.

Conclusions Manipulation of the microbiome of I. ricinus larvae had no effect on their ability to acquire B. afzelii. In contrast, B. afzelii infection in the mouse had dramatic effects on the composition of the gut microbiome in I. ricinus nymphs. Our study demonstrates that vector-borne infections in the vertebrate host shape the microbiome of the arthropod vector.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted March 15, 2021.
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Borrelia infection in rodent host has dramatic effects on the microbiome of ticks
Phineas T. Hamilton, Elodie Maluenda, Anouk Sarr, Alessandro Belli, Georgia Hurry, Olivier Duron, Olivier Plantard, Maarten J. Voordouw
bioRxiv 2021.03.15.435198; doi: https://doi.org/10.1101/2021.03.15.435198
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Borrelia infection in rodent host has dramatic effects on the microbiome of ticks
Phineas T. Hamilton, Elodie Maluenda, Anouk Sarr, Alessandro Belli, Georgia Hurry, Olivier Duron, Olivier Plantard, Maarten J. Voordouw
bioRxiv 2021.03.15.435198; doi: https://doi.org/10.1101/2021.03.15.435198

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