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Ecological Contacts and Host Specificity Promote Replacement of Nutritional Endosymbionts in Ticks

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Abstract

Symbiosis with vitamin-provisioning microbes is essential for the nutrition of animals with some specialized feeding habits. While coevolution favors the interdependence between symbiotic partners, their associations are not necessarily stable: Recently acquired symbionts can replace ancestral symbionts. In this study, we demonstrate successful replacement by Francisella-like endosymbionts (-LE), a group of B-vitamin-provisioning endosymbionts, across tick communities driven by horizontal transfers. Using a broad collection of Francisella-LE-infected tick species, we determined the diversity of Francisella-LE haplotypes through a multi-locus strain typing approach and further characterized their phylogenetic relationships and their association with biological traits of their tick hosts. The patterns observed showed that Francisella-LE commonly transfer through similar ecological networks and geographic distributions shared among different tick species and, in certain cases, through preferential shuffling across congeneric tick species. Altogether, these findings reveal the importance of geographic, ecological, and phylogenetic proximity in shaping the replacement pattern in which new nutritional symbioses are initiated.

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Fig. 1
Fig. 2

adapted from Burger et al. [34], and all congeneric tick species were arbitrarily considered as equally distant

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Data Availability

Nucleotide sequences of Francisella-LE were deposited in the GenBank nucleotide database (16S rRNA: MW287912-MW287986; rpoB: MW286019-MW286093; groEL: MW285869-MW285943; ftsZ: MW285794-MW285868; gyrB: MW285944-MW286018).

Code Availability

Scripts used for the statistical analyses are available on GitHub (https://github.com/mariebuysse/pending).

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Acknowledgements

We thank D. Ayala, C. Chevillon, F. Delsuc, B. de Thoisy, S. Garnier, H. Hawlena, Q. Lejarre, K. McCoy, C. Paupy, O. Plantard, N. Rahola, S. Moutailler, C. Galon, and L. Vial.

Funding

This work has benefited from (1) an international grant (EVOSYM) co-managed by the Ministry of Science, Technology and Space (Israel) and the Centre National de la Recherche Scientifique (CNRS, France), from (2) “Investissements d’Avenir” managed by the Agence Nationale de la Recherche (ANR, France, Laboratoire d’Excellence CEBA, ANR-10-LABX-25–01), and from (3) the Israel Science Foundation (ISF grant No. 1074/18).

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Author notes

  1. Yuval Gottlieb and Olivier Duron Contributed equally to this work

Authors and Affiliations

  1. Maladies Infectieuses et Vecteurs : Ecologie, Génétique, Evolution et Contrôle), Centre National de la Recherche Scientifique (CNRS) - Institut pour la Recherche et le Développement (IRD), Université de Montpellier (UM), Montpellier, France

    Marie Buysse, Florian Binetruy & Olivier Duron

  2. CREES (Centre de Recherche en Écologie et Évolution de la Santé), Montpellier, France

    Marie Buysse & Olivier Duron

  3. Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

    Raz Leibson & Yuval Gottlieb

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  1. Marie Buysse
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  2. Florian Binetruy
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  3. Raz Leibson
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  4. Yuval Gottlieb
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  5. Olivier Duron
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Contributions

Y.G. and O.D. designed the study. M.B., Y.G., and O.D. wrote the manuscript. M.B., F.B., and R.L. performed the molecular typing. M.B. and O.D. performed the phylogenetic and statistical analyses. All authors agreed on the final version of the manuscript.

Corresponding authors

Correspondence to Marie Buysse, Yuval Gottlieb or Olivier Duron.

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Buysse, M., Binetruy, F., Leibson, R. et al. Ecological Contacts and Host Specificity Promote Replacement of Nutritional Endosymbionts in Ticks. Microb Ecol 83, 776–788 (2022). https://doi.org/10.1007/s00248-021-01773-0

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