A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum

Marie Buysse*, Anna Maria Floriano, Yuval Gottlieb, Tiago Nardi, Francesco Comandatore, Emanuela Olivieri, Alessia Giannetto, Ana M. Palomar, Benjamin L. Makepeace, Chiara Bazzocchi, Alessandra Cafiso, Davide Sassera, Olivier Duron

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

20 Scopus citations

Abstract

Many animals are dependent on microbial partners that provide essential nutrients lacking from their diet. Ticks, whose diet consists exclusively on vertebrate blood, rely on maternally inherited bacterial symbionts to supply B vitamins. While previously studied tick species consis-tently harbor a single lineage of those nutritional symbionts, we evidence here that the invasive tick Hyalomma marginatum harbors a unique dual-partner nutritional system between an ancestral symbiont, Francisella, and a more recently acquired symbiont, Midichloria. Using metagenomics, we show that Francisella exhibits extensive genome erosion that endangers the nutritional symbiotic interactions. Its genome includes folate and riboflavin biosynthesis pathways but deprived functional biotin biosynthesis on account of massive pseudogenization. Co-symbiosis compensates this deficiency since the Midichloria genome encompasses an intact biotin operon, which was primarily acquired via lateral gene transfer from unrelated intracellular bacteria commonly infecting arthro-pods. Thus, in H. marginatum, a mosaic of co-evolved symbionts incorporating gene combinations of distant phylogenetic origins emerged to prevent the collapse of an ancestral nutritional symbiosis. Such dual endosymbiosis was never reported in other blood feeders but was recently documented in agricultural pests feeding on plant sap, suggesting that it may be a key mechanism for advanced adaptation of arthropods to specialized diets.

Original languageAmerican English
Article numbere72747
JournaleLife
Volume10
DOIs
StatePublished - Dec 2021

Bibliographical note

Funding Information:
The authors are grateful to Tal Azagi for tick collection and extraction and Inbar Plaschkes for initial sequence analysis of the Israeli sample, to Justine Grillet, Valentina Serra, and Catherine Hartley for technical support during molecular analyses. This work benefited from (1) an international ‘Joint Research Projects’ 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) The Israel Science Foundation (ISF Grant no. 1074/18), from (3) the Human Frontier Science Programme Grant RGY0075/2017 to DS, and the Italian Ministry of Education, University and Research (MIUR): Dipartimenti di Eccellenza Programme (2018–2022) – Department of Biology and Biotechnology ‘L. Spallanzani,’ University of Pavia to DS, and from (4) the French Agence Nationale de la Recherche (ANR-21-CE02-0002).

Funding Information:
Ministry of Science, Technology and Space Centre National de la Recherche Scientifique EVOSYM EVOSYM Yuval Gottlieb Olivier Duron Israel Science Foundation 1074/18 Yuval Gottlieb Human Frontier Science Program Ministry of Education, University and Research Centre National de la Recherche Scientifique RGY0075/2017 ANR-21-CE02-0002 Davide Sassera Davide Sassera Olivier Duron.

Publisher Copyright:
© Buysse et al.

Keywords

  • endosymbiosis
  • hematophagy
  • Francisella
  • Midichloria
  • Hyalomma
  • Other

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