Genome sequences of four Ixodes species expands understanding of tick evolution

Abstract Background Ticks, hematophagous Acari, pose a significant threat by transmitting various pathogens to their vertebrate hosts during feeding. Despite advances in tick genomics, high-quality genomes were lacking until recently, particularly in the genus Ixodes, which includes the main vectors...

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Main Authors: Alexandra Cerqueira de Araujo, Benjamin Noel, Anthony Bretaudeau, Karine Labadie, Matéo Boudet, Nachida Tadrent, Benjamin Istace, Salima Kritli, Corinne Cruaud, Robert Olaso, Jean-François Deleuze, Maarten J. Voordouw, Caroline Hervet, Olivier Plantard, Aya Zamoto-Niikura, Thomas Chertemps, Martine Maïbèche, Frédérique Hilliou, Gaëlle Le Goff, Jindřich Chmelař, Vilém Mazák, Mohamed Amine Jmel, Michalis Kotsyfakis, José María Medina, Michael Hackenberg, Ladislav Šimo, Fotini A. Koutroumpa, Patrick Wincker, Petr Kopáček, Jan Perner, Jean-Marc Aury, Claude Rispe
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Biology
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Online Access:https://doi.org/10.1186/s12915-025-02121-1
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author Alexandra Cerqueira de Araujo
Benjamin Noel
Anthony Bretaudeau
Karine Labadie
Matéo Boudet
Nachida Tadrent
Benjamin Istace
Salima Kritli
Corinne Cruaud
Robert Olaso
Jean-François Deleuze
Maarten J. Voordouw
Caroline Hervet
Olivier Plantard
Aya Zamoto-Niikura
Thomas Chertemps
Martine Maïbèche
Frédérique Hilliou
Gaëlle Le Goff
Jindřich Chmelař
Vilém Mazák
Mohamed Amine Jmel
Michalis Kotsyfakis
José María Medina
Michael Hackenberg
Ladislav Šimo
Fotini A. Koutroumpa
Patrick Wincker
Petr Kopáček
Jan Perner
Jean-Marc Aury
Claude Rispe
author_facet Alexandra Cerqueira de Araujo
Benjamin Noel
Anthony Bretaudeau
Karine Labadie
Matéo Boudet
Nachida Tadrent
Benjamin Istace
Salima Kritli
Corinne Cruaud
Robert Olaso
Jean-François Deleuze
Maarten J. Voordouw
Caroline Hervet
Olivier Plantard
Aya Zamoto-Niikura
Thomas Chertemps
Martine Maïbèche
Frédérique Hilliou
Gaëlle Le Goff
Jindřich Chmelař
Vilém Mazák
Mohamed Amine Jmel
Michalis Kotsyfakis
José María Medina
Michael Hackenberg
Ladislav Šimo
Fotini A. Koutroumpa
Patrick Wincker
Petr Kopáček
Jan Perner
Jean-Marc Aury
Claude Rispe
author_sort Alexandra Cerqueira de Araujo
collection DOAJ
description Abstract Background Ticks, hematophagous Acari, pose a significant threat by transmitting various pathogens to their vertebrate hosts during feeding. Despite advances in tick genomics, high-quality genomes were lacking until recently, particularly in the genus Ixodes, which includes the main vectors of Lyme disease. Results Here, we present the genome sequences of four tick species, derived from a single female individual, with a particular focus on the European species Ixodes ricinus, achieving a chromosome-level assembly. Additionally, draft assemblies were generated for the three other Ixodes species, I. persulcatus, I. pacificus, and I. hexagonus. The quality of the four genomes and extensive annotation of several important gene families have allowed us to study the evolution of gene repertoires at the level of the genus Ixodes and of the tick group. We have determined gene families that have undergone major amplifications during the evolution of ticks, while an expression atlas obtained for I. ricinus reveals striking patterns of specialization both between and within gene families. Notably, several gene family amplifications are associated with a proliferation of single-exon genes—most strikingly for fatty acid elongases and sulfotransferases. Conclusions The integration of our data with existing genomes establishes a solid framework for the study of gene evolution, improving our understanding of tick biology. In addition, our work lays the foundations for applied research and innovative control targeting these organisms.
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spelling doaj-art-62b83288daae4ec3906bc15e122c692c2025-01-26T12:52:41ZengBMCBMC Biology1741-70072025-01-0123112910.1186/s12915-025-02121-1Genome sequences of four Ixodes species expands understanding of tick evolutionAlexandra Cerqueira de Araujo0Benjamin Noel1Anthony Bretaudeau2Karine Labadie3Matéo Boudet4Nachida Tadrent5Benjamin Istace6Salima Kritli7Corinne Cruaud8Robert Olaso9Jean-François Deleuze10Maarten J. Voordouw11Caroline Hervet12Olivier Plantard13Aya Zamoto-Niikura14Thomas Chertemps15Martine Maïbèche16Frédérique Hilliou17Gaëlle Le Goff18Jindřich Chmelař19Vilém Mazák20Mohamed Amine Jmel21Michalis Kotsyfakis22José María Medina23Michael Hackenberg24Ladislav Šimo25Fotini A. Koutroumpa26Patrick Wincker27Petr Kopáček28Jan Perner29Jean-Marc Aury30Claude Rispe31Oniris, INRAE, BIOEPARGénomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-SaclayUniversity of Rennes, INRIA, CNRS, IRISAGenoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-SaclayUniversity of Rennes, INRIA, CNRS, IRISAGénomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-SaclayGénomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-SaclayGénomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-SaclayGenoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-SaclayCentre National de Recherche en Génomique Humaine (CNRGH), Institut de Biologie François Jacob, CEA, Université Paris-SaclayCentre National de Recherche en Génomique Humaine (CNRGH), Institut de Biologie François Jacob, CEA, Université Paris-SaclayDepartment of Veterinary Microbiology, Western College of Veterinary Medicine, University of SaskatchewanOniris, INRAE, BIOEPAROniris, INRAE, BIOEPARResearch Center for Biosafety, Laboratory Animal and Pathogen Bank, National Institute of Infectious DiseasesInstitut d’Ecologie Et Des Sciences de L’Environnement de Paris, Sorbonne Université, INRAE, CNRS, IRD, UPECInstitut d’Ecologie Et Des Sciences de L’Environnement de Paris, Sorbonne Université, INRAE, CNRS, IRD, UPECUniversité Côte d’Azur, INRAE, CNRS, ISAUniversité Côte d’Azur, INRAE, CNRS, ISADepartment of Medical Biology, Faculty of Science, University of South Bohemia in České BudějoviceDepartment of Medical Biology, Faculty of Science, University of South Bohemia in České BudějoviceInstitute of Parasitology, Biology Centre, Czech Academy of SciencesInstitute of Parasitology, Biology Centre, Czech Academy of SciencesDpto. de Genética, Facultad de Ciencias, Universidad de GranadaDpto. de Genética, Facultad de Ciencias, Universidad de GranadaANSES, INRAE, Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, Laboratoire de Santé AnimaleINRAE, Université de Tours, UMR1282 Infectiologie Et Santé PubliqueGénomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-SaclayInstitute of Parasitology, Biology Centre, Czech Academy of SciencesInstitute of Parasitology, Biology Centre, Czech Academy of SciencesGénomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-SaclayOniris, INRAE, BIOEPARAbstract Background Ticks, hematophagous Acari, pose a significant threat by transmitting various pathogens to their vertebrate hosts during feeding. Despite advances in tick genomics, high-quality genomes were lacking until recently, particularly in the genus Ixodes, which includes the main vectors of Lyme disease. Results Here, we present the genome sequences of four tick species, derived from a single female individual, with a particular focus on the European species Ixodes ricinus, achieving a chromosome-level assembly. Additionally, draft assemblies were generated for the three other Ixodes species, I. persulcatus, I. pacificus, and I. hexagonus. The quality of the four genomes and extensive annotation of several important gene families have allowed us to study the evolution of gene repertoires at the level of the genus Ixodes and of the tick group. We have determined gene families that have undergone major amplifications during the evolution of ticks, while an expression atlas obtained for I. ricinus reveals striking patterns of specialization both between and within gene families. Notably, several gene family amplifications are associated with a proliferation of single-exon genes—most strikingly for fatty acid elongases and sulfotransferases. Conclusions The integration of our data with existing genomes establishes a solid framework for the study of gene evolution, improving our understanding of tick biology. In addition, our work lays the foundations for applied research and innovative control targeting these organisms.https://doi.org/10.1186/s12915-025-02121-1Comparative genomicsParasiteHematophagyDuplicationRetroposition
spellingShingle Alexandra Cerqueira de Araujo
Benjamin Noel
Anthony Bretaudeau
Karine Labadie
Matéo Boudet
Nachida Tadrent
Benjamin Istace
Salima Kritli
Corinne Cruaud
Robert Olaso
Jean-François Deleuze
Maarten J. Voordouw
Caroline Hervet
Olivier Plantard
Aya Zamoto-Niikura
Thomas Chertemps
Martine Maïbèche
Frédérique Hilliou
Gaëlle Le Goff
Jindřich Chmelař
Vilém Mazák
Mohamed Amine Jmel
Michalis Kotsyfakis
José María Medina
Michael Hackenberg
Ladislav Šimo
Fotini A. Koutroumpa
Patrick Wincker
Petr Kopáček
Jan Perner
Jean-Marc Aury
Claude Rispe
Genome sequences of four Ixodes species expands understanding of tick evolution
BMC Biology
Comparative genomics
Parasite
Hematophagy
Duplication
Retroposition
title Genome sequences of four Ixodes species expands understanding of tick evolution
title_full Genome sequences of four Ixodes species expands understanding of tick evolution
title_fullStr Genome sequences of four Ixodes species expands understanding of tick evolution
title_full_unstemmed Genome sequences of four Ixodes species expands understanding of tick evolution
title_short Genome sequences of four Ixodes species expands understanding of tick evolution
title_sort genome sequences of four ixodes species expands understanding of tick evolution
topic Comparative genomics
Parasite
Hematophagy
Duplication
Retroposition
url https://doi.org/10.1186/s12915-025-02121-1
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