The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii
Q fever is a highly infectious disease with a worldwide distribution. Its causative agent, the intracellular bacterium Coxiella burnetii, infects a variety of vertebrate species, including humans. Its evolutionary origin remains almost entirely unknown and uncertainty persists regarding the identity and lifestyle of its ancestors. A few tick species were recently found to harbor maternally-inherited Coxiella-like organisms engaged in symbiotic interactions, but their relationships to the Q fever pathogen remain unclear. Here, we extensively sampled ticks, identifying new and atypical Coxiella strains from 40 of 58 examined species, and used this data to infer the evolutionary processes leading to the emergence of C. burnetii. Phylogenetic analyses of multi-locus typing and whole-genome sequencing data revealed that Coxiella-like organisms represent an ancient and monophyletic group allied to ticks. Remarkably, all known C. burnetii strains originate within this group and are the descendants of a Coxiella-like progenitor hosted by ticks. Using both colony-reared and field-collected gravid females, we further establish the presence of highly efficient maternal transmission of these Coxiella -like organisms in four examined tick species, a pattern coherent with an endosymbiotic lifestyle. Our laboratory culture assays also showed that these Coxiella -like organisms were not amenable to culture in the vertebrate cell environment, suggesting dif- ferent metabolic requirements compared to C . burnetii . Altogether, this corpus of data dem- onstrates that C . burnetii recently evolved from an inherited symbiont of ticks which succeeded in infecting vertebrate cells, likely by the acquisition of novel virulence factors.
Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , |
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Format: | article biblioteca |
Language: | eng |
Subjects: | L73 - Maladies des animaux, L72 - Organismes nuisibles des animaux, Coxiella burnetii, évolution, symbiote, fièvre Q, Rhipicephalus, relation hôte pathogène, virulence, vertébré, variation génétique, héritabilité, femelle, http://aims.fao.org/aos/agrovoc/c_36027, http://aims.fao.org/aos/agrovoc/c_2745, http://aims.fao.org/aos/agrovoc/c_7562, http://aims.fao.org/aos/agrovoc/c_16461, http://aims.fao.org/aos/agrovoc/c_6560, http://aims.fao.org/aos/agrovoc/c_34017, http://aims.fao.org/aos/agrovoc/c_8261, http://aims.fao.org/aos/agrovoc/c_8196, http://aims.fao.org/aos/agrovoc/c_15975, http://aims.fao.org/aos/agrovoc/c_3570, http://aims.fao.org/aos/agrovoc/c_15969, |
Online Access: | http://agritrop.cirad.fr/576646/ http://agritrop.cirad.fr/576646/1/576646.pdf |
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L73 - Maladies des animaux L72 - Organismes nuisibles des animaux Coxiella burnetii évolution symbiote fièvre Q Rhipicephalus relation hôte pathogène virulence vertébré variation génétique héritabilité femelle http://aims.fao.org/aos/agrovoc/c_36027 http://aims.fao.org/aos/agrovoc/c_2745 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_16461 http://aims.fao.org/aos/agrovoc/c_6560 http://aims.fao.org/aos/agrovoc/c_34017 http://aims.fao.org/aos/agrovoc/c_8261 http://aims.fao.org/aos/agrovoc/c_8196 http://aims.fao.org/aos/agrovoc/c_15975 http://aims.fao.org/aos/agrovoc/c_3570 http://aims.fao.org/aos/agrovoc/c_15969 L73 - Maladies des animaux L72 - Organismes nuisibles des animaux Coxiella burnetii évolution symbiote fièvre Q Rhipicephalus relation hôte pathogène virulence vertébré variation génétique héritabilité femelle http://aims.fao.org/aos/agrovoc/c_36027 http://aims.fao.org/aos/agrovoc/c_2745 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_16461 http://aims.fao.org/aos/agrovoc/c_6560 http://aims.fao.org/aos/agrovoc/c_34017 http://aims.fao.org/aos/agrovoc/c_8261 http://aims.fao.org/aos/agrovoc/c_8196 http://aims.fao.org/aos/agrovoc/c_15975 http://aims.fao.org/aos/agrovoc/c_3570 http://aims.fao.org/aos/agrovoc/c_15969 |
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L73 - Maladies des animaux L72 - Organismes nuisibles des animaux Coxiella burnetii évolution symbiote fièvre Q Rhipicephalus relation hôte pathogène virulence vertébré variation génétique héritabilité femelle http://aims.fao.org/aos/agrovoc/c_36027 http://aims.fao.org/aos/agrovoc/c_2745 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_16461 http://aims.fao.org/aos/agrovoc/c_6560 http://aims.fao.org/aos/agrovoc/c_34017 http://aims.fao.org/aos/agrovoc/c_8261 http://aims.fao.org/aos/agrovoc/c_8196 http://aims.fao.org/aos/agrovoc/c_15975 http://aims.fao.org/aos/agrovoc/c_3570 http://aims.fao.org/aos/agrovoc/c_15969 L73 - Maladies des animaux L72 - Organismes nuisibles des animaux Coxiella burnetii évolution symbiote fièvre Q Rhipicephalus relation hôte pathogène virulence vertébré variation génétique héritabilité femelle http://aims.fao.org/aos/agrovoc/c_36027 http://aims.fao.org/aos/agrovoc/c_2745 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_16461 http://aims.fao.org/aos/agrovoc/c_6560 http://aims.fao.org/aos/agrovoc/c_34017 http://aims.fao.org/aos/agrovoc/c_8261 http://aims.fao.org/aos/agrovoc/c_8196 http://aims.fao.org/aos/agrovoc/c_15975 http://aims.fao.org/aos/agrovoc/c_3570 http://aims.fao.org/aos/agrovoc/c_15969 Duron, Olivier Noel, Valérie McCoy, Karen D. Bonazzi, Matteo Sidi-Boumedine, Karim Morel, Olivier Vavre, Fabrice Zenner, Lionel Jourdain, Elsa Durand, Patrick Arnathau, Céline Renaud, François Trape, Jean-François Biguezoton, Abel S. Cremaschi, Julie Dietrich, Muriel Leger, Elsa Appelgren, Anaïs Dupraz, Marlene Gómez-Díaz, Elena Diatta, Georges Dayo, Guiguigbaza Kossigan Adakal, Hassane Zoungrana, Adrien Vial, Laurence Chevillon, Christine The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii |
description |
Q fever is a highly infectious disease with a worldwide distribution. Its causative agent, the intracellular bacterium Coxiella burnetii, infects a variety of vertebrate species, including humans. Its evolutionary origin remains almost entirely unknown and uncertainty persists regarding the identity and lifestyle of its ancestors. A few tick species were recently found to harbor maternally-inherited Coxiella-like organisms engaged in symbiotic interactions, but their relationships to the Q fever pathogen remain unclear. Here, we extensively sampled ticks, identifying new and atypical Coxiella strains from 40 of 58 examined species, and used this data to infer the evolutionary processes leading to the emergence of C. burnetii. Phylogenetic analyses of multi-locus typing and whole-genome sequencing data revealed that Coxiella-like organisms represent an ancient and monophyletic group allied to ticks. Remarkably, all known C. burnetii strains originate within this group and are the descendants of a Coxiella-like progenitor hosted by ticks. Using both colony-reared and field-collected gravid females, we further establish the presence of highly efficient maternal transmission of these Coxiella -like organisms in four examined tick species, a pattern coherent with an endosymbiotic lifestyle. Our laboratory culture assays also showed that these Coxiella -like organisms were not amenable to culture in the vertebrate cell environment, suggesting dif- ferent metabolic requirements compared to C . burnetii . Altogether, this corpus of data dem- onstrates that C . burnetii recently evolved from an inherited symbiont of ticks which succeeded in infecting vertebrate cells, likely by the acquisition of novel virulence factors. |
format |
article |
topic_facet |
L73 - Maladies des animaux L72 - Organismes nuisibles des animaux Coxiella burnetii évolution symbiote fièvre Q Rhipicephalus relation hôte pathogène virulence vertébré variation génétique héritabilité femelle http://aims.fao.org/aos/agrovoc/c_36027 http://aims.fao.org/aos/agrovoc/c_2745 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_16461 http://aims.fao.org/aos/agrovoc/c_6560 http://aims.fao.org/aos/agrovoc/c_34017 http://aims.fao.org/aos/agrovoc/c_8261 http://aims.fao.org/aos/agrovoc/c_8196 http://aims.fao.org/aos/agrovoc/c_15975 http://aims.fao.org/aos/agrovoc/c_3570 http://aims.fao.org/aos/agrovoc/c_15969 |
author |
Duron, Olivier Noel, Valérie McCoy, Karen D. Bonazzi, Matteo Sidi-Boumedine, Karim Morel, Olivier Vavre, Fabrice Zenner, Lionel Jourdain, Elsa Durand, Patrick Arnathau, Céline Renaud, François Trape, Jean-François Biguezoton, Abel S. Cremaschi, Julie Dietrich, Muriel Leger, Elsa Appelgren, Anaïs Dupraz, Marlene Gómez-Díaz, Elena Diatta, Georges Dayo, Guiguigbaza Kossigan Adakal, Hassane Zoungrana, Adrien Vial, Laurence Chevillon, Christine |
author_facet |
Duron, Olivier Noel, Valérie McCoy, Karen D. Bonazzi, Matteo Sidi-Boumedine, Karim Morel, Olivier Vavre, Fabrice Zenner, Lionel Jourdain, Elsa Durand, Patrick Arnathau, Céline Renaud, François Trape, Jean-François Biguezoton, Abel S. Cremaschi, Julie Dietrich, Muriel Leger, Elsa Appelgren, Anaïs Dupraz, Marlene Gómez-Díaz, Elena Diatta, Georges Dayo, Guiguigbaza Kossigan Adakal, Hassane Zoungrana, Adrien Vial, Laurence Chevillon, Christine |
author_sort |
Duron, Olivier |
title |
The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii |
title_short |
The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii |
title_full |
The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii |
title_fullStr |
The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii |
title_full_unstemmed |
The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii |
title_sort |
recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the q fever pathogen, coxiella burnetii |
url |
http://agritrop.cirad.fr/576646/ http://agritrop.cirad.fr/576646/1/576646.pdf |
work_keys_str_mv |
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dig-cirad-fr-5766462024-01-28T22:47:29Z http://agritrop.cirad.fr/576646/ http://agritrop.cirad.fr/576646/ The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii. Duron Olivier, Noel Valérie, McCoy Karen D., Bonazzi Matteo, Sidi-Boumedine Karim, Morel Olivier, Vavre Fabrice, Zenner Lionel, Jourdain Elsa, Durand Patrick, Arnathau Céline, Renaud François, Trape Jean-François, Biguezoton Abel S., Cremaschi Julie, Dietrich Muriel, Leger Elsa, Appelgren Anaïs, Dupraz Marlene, Gómez-Díaz Elena, Diatta Georges, Dayo Guiguigbaza Kossigan, Adakal Hassane, Zoungrana Adrien, Vial Laurence, Chevillon Christine. 2015. PLoS Pathogens, 11 (5):e1004892, 23 p.https://doi.org/10.1371/journal.ppat.1004892 <https://doi.org/10.1371/journal.ppat.1004892> The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii Duron, Olivier Noel, Valérie McCoy, Karen D. Bonazzi, Matteo Sidi-Boumedine, Karim Morel, Olivier Vavre, Fabrice Zenner, Lionel Jourdain, Elsa Durand, Patrick Arnathau, Céline Renaud, François Trape, Jean-François Biguezoton, Abel S. Cremaschi, Julie Dietrich, Muriel Leger, Elsa Appelgren, Anaïs Dupraz, Marlene Gómez-Díaz, Elena Diatta, Georges Dayo, Guiguigbaza Kossigan Adakal, Hassane Zoungrana, Adrien Vial, Laurence Chevillon, Christine eng 2015 PLoS Pathogens L73 - Maladies des animaux L72 - Organismes nuisibles des animaux Coxiella burnetii évolution symbiote fièvre Q Rhipicephalus relation hôte pathogène virulence vertébré variation génétique héritabilité femelle http://aims.fao.org/aos/agrovoc/c_36027 http://aims.fao.org/aos/agrovoc/c_2745 http://aims.fao.org/aos/agrovoc/c_7562 http://aims.fao.org/aos/agrovoc/c_16461 http://aims.fao.org/aos/agrovoc/c_6560 http://aims.fao.org/aos/agrovoc/c_34017 http://aims.fao.org/aos/agrovoc/c_8261 http://aims.fao.org/aos/agrovoc/c_8196 http://aims.fao.org/aos/agrovoc/c_15975 http://aims.fao.org/aos/agrovoc/c_3570 http://aims.fao.org/aos/agrovoc/c_15969 Q fever is a highly infectious disease with a worldwide distribution. Its causative agent, the intracellular bacterium Coxiella burnetii, infects a variety of vertebrate species, including humans. Its evolutionary origin remains almost entirely unknown and uncertainty persists regarding the identity and lifestyle of its ancestors. A few tick species were recently found to harbor maternally-inherited Coxiella-like organisms engaged in symbiotic interactions, but their relationships to the Q fever pathogen remain unclear. Here, we extensively sampled ticks, identifying new and atypical Coxiella strains from 40 of 58 examined species, and used this data to infer the evolutionary processes leading to the emergence of C. burnetii. Phylogenetic analyses of multi-locus typing and whole-genome sequencing data revealed that Coxiella-like organisms represent an ancient and monophyletic group allied to ticks. Remarkably, all known C. burnetii strains originate within this group and are the descendants of a Coxiella-like progenitor hosted by ticks. Using both colony-reared and field-collected gravid females, we further establish the presence of highly efficient maternal transmission of these Coxiella -like organisms in four examined tick species, a pattern coherent with an endosymbiotic lifestyle. Our laboratory culture assays also showed that these Coxiella -like organisms were not amenable to culture in the vertebrate cell environment, suggesting dif- ferent metabolic requirements compared to C . burnetii . Altogether, this corpus of data dem- onstrates that C . burnetii recently evolved from an inherited symbiont of ticks which succeeded in infecting vertebrate cells, likely by the acquisition of novel virulence factors. article info:eu-repo/semantics/article Journal Article info:eu-repo/semantics/publishedVersion http://agritrop.cirad.fr/576646/1/576646.pdf text cc_by info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by/4.0/ https://doi.org/10.1371/journal.ppat.1004892 10.1371/journal.ppat.1004892 info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.ppat.1004892 info:eu-repo/semantics/altIdentifier/purl/https://doi.org/10.1371/journal.ppat.1004892 info:eu-repo/semantics/dataset/purl/http://www.ncbi.nlm.nih.gov/nuccore/KP994768 info:eu-repo/semantics/dataset/purl/http://www.ncbi.nlm.nih.gov/nuccore/KP994678 info:eu-repo/semantics/dataset/purl/http://www.ncbi.nlm.nih.gov/nuccore/KP985445 info:eu-repo/semantics/dataset/purl/http://www.ncbi.nlm.nih.gov/nuccore/KP985265 info:eu-repo/semantics/dataset/purl/http://www.ncbi.nlm.nih.gov/nuccore/KP985358 |