Evolutionary changes in symbiont community structure in ticks

Autores
Duron, Olivier; Binetruy, Florian; Noël, Valérie; Cremaschi, Julie; McCoy, Karen D.; Arnathau, Céline; Plantard, Olivier; Goolsby, John; Pérez de León, Adalberto A.; Heylen, Dieter J. A.; Van Oosten, A. Raoul; Gottlieb, Yuval; Baneth, Gad; Guglielmone, Alberto Alejandro; Estrada Peña, Agustin; Opara, Maxwell N.; Zenner, Lionel; Vavre, Fabrice; Chevillon, Christine
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Ecological specialization to restricted diet niches is driven by obligate, and often maternally inherited, symbionts in many arthropod lineages. These heritable symbionts typically form evolutionarily stable associations with arthropods that can last for millions of years. Ticks were recently found to harbour such an obligate symbiont, Coxiella-LE, that synthesizes B vitamins and cofactors not obtained in sufficient quantities from blood diet. In this study, the examination of 81 tick species shows that some Coxiella-LE symbioses are evolutionarily stable with an ancient acquisition followed by codiversification as observed in ticks belonging to the Rhipicephalus genus. However, many other Coxiella-LE symbioses are characterized by low evolutionary stability with frequent host shifts and extinction events. Further examination revealed the presence of nine other genera of maternally inherited bacteria in ticks. Although these nine symbionts were primarily thought to be facultative, their distribution among tick species rather suggests that at least four may have independently replaced Coxiella-LE and likely represent alternative obligate symbionts. Phylogenetic evidence otherwise indicates that cocladogenesis is globally rare in these symbioses as most originate via horizontal transfer of an existing symbiont between unrelated tick species. As a result, the structure of these symbiont communities is not fixed and stable across the tick phylogeny. Most importantly, the symbiont communities commonly reach high levels of diversity with up to six unrelated maternally inherited bacteria coexisting within host species. We further conjecture that interactions among coexisting symbionts are pivotal drivers of community structure both among and within tick species.
Fil: Duron, Olivier. Centre National de la Recherche Scientifique; Francia
Fil: Binetruy, Florian. Centre National de la Recherche Scientifique; Francia
Fil: Noël, Valérie. Centre National de la Recherche Scientifique; Francia
Fil: Cremaschi, Julie. Centre National de la Recherche Scientifique; Francia
Fil: McCoy, Karen D.. Centre National de la Recherche Scientifique; Francia
Fil: Arnathau, Céline. Centre National de la Recherche Scientifique; Francia
Fil: Plantard, Olivier. Institut National de la Recherche Agronomique; Francia
Fil: Goolsby, John. United States Department of Agriculture. Agriculture Research Service; Estados Unidos
Fil: Pérez de León, Adalberto A.. Veterinary Pest Genomics Center; Estados Unidos
Fil: Heylen, Dieter J. A.. Universiteit Antwerp; Bélgica
Fil: Van Oosten, A. Raoul. Universiteit Antwerp; Bélgica
Fil: Gottlieb, Yuval. The Hebrew University of Jerusalem; Israel
Fil: Baneth, Gad. The Hebrew University of Jerusalem; Israel
Fil: Guglielmone, Alberto Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Regional Buenos Aires; Argentina
Fil: Estrada Peña, Agustin. Universidad de Zaragoza; España
Fil: Opara, Maxwell N.. University Of Abuja; Nigeria
Fil: Zenner, Lionel. Centre National de la Recherche Scientifique; Francia
Fil: Vavre, Fabrice. Centre National de la Recherche Scientifique; Francia
Fil: Chevillon, Christine. Centre National de la Recherche Scientifique; Francia
Materia
Co-Evolution
Heritable Symbiont Communities
Maternally Inherited Bacteria
Symbiosis
Tick
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/58622

id CONICETDig_1dabf8c0f6c6adb3383726c49352e31d
oai_identifier_str oai:ri.conicet.gov.ar:11336/58622
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Evolutionary changes in symbiont community structure in ticksDuron, OlivierBinetruy, FlorianNoël, ValérieCremaschi, JulieMcCoy, Karen D.Arnathau, CélinePlantard, OlivierGoolsby, JohnPérez de León, Adalberto A.Heylen, Dieter J. A.Van Oosten, A. RaoulGottlieb, YuvalBaneth, GadGuglielmone, Alberto AlejandroEstrada Peña, AgustinOpara, Maxwell N.Zenner, LionelVavre, FabriceChevillon, ChristineCo-EvolutionHeritable Symbiont CommunitiesMaternally Inherited BacteriaSymbiosisTickhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Ecological specialization to restricted diet niches is driven by obligate, and often maternally inherited, symbionts in many arthropod lineages. These heritable symbionts typically form evolutionarily stable associations with arthropods that can last for millions of years. Ticks were recently found to harbour such an obligate symbiont, Coxiella-LE, that synthesizes B vitamins and cofactors not obtained in sufficient quantities from blood diet. In this study, the examination of 81 tick species shows that some Coxiella-LE symbioses are evolutionarily stable with an ancient acquisition followed by codiversification as observed in ticks belonging to the Rhipicephalus genus. However, many other Coxiella-LE symbioses are characterized by low evolutionary stability with frequent host shifts and extinction events. Further examination revealed the presence of nine other genera of maternally inherited bacteria in ticks. Although these nine symbionts were primarily thought to be facultative, their distribution among tick species rather suggests that at least four may have independently replaced Coxiella-LE and likely represent alternative obligate symbionts. Phylogenetic evidence otherwise indicates that cocladogenesis is globally rare in these symbioses as most originate via horizontal transfer of an existing symbiont between unrelated tick species. As a result, the structure of these symbiont communities is not fixed and stable across the tick phylogeny. Most importantly, the symbiont communities commonly reach high levels of diversity with up to six unrelated maternally inherited bacteria coexisting within host species. We further conjecture that interactions among coexisting symbionts are pivotal drivers of community structure both among and within tick species.Fil: Duron, Olivier. Centre National de la Recherche Scientifique; FranciaFil: Binetruy, Florian. Centre National de la Recherche Scientifique; FranciaFil: Noël, Valérie. Centre National de la Recherche Scientifique; FranciaFil: Cremaschi, Julie. Centre National de la Recherche Scientifique; FranciaFil: McCoy, Karen D.. Centre National de la Recherche Scientifique; FranciaFil: Arnathau, Céline. Centre National de la Recherche Scientifique; FranciaFil: Plantard, Olivier. Institut National de la Recherche Agronomique; FranciaFil: Goolsby, John. United States Department of Agriculture. Agriculture Research Service; Estados UnidosFil: Pérez de León, Adalberto A.. Veterinary Pest Genomics Center; Estados UnidosFil: Heylen, Dieter J. A.. Universiteit Antwerp; BélgicaFil: Van Oosten, A. Raoul. Universiteit Antwerp; BélgicaFil: Gottlieb, Yuval. The Hebrew University of Jerusalem; IsraelFil: Baneth, Gad. The Hebrew University of Jerusalem; IsraelFil: Guglielmone, Alberto Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Regional Buenos Aires; ArgentinaFil: Estrada Peña, Agustin. Universidad de Zaragoza; EspañaFil: Opara, Maxwell N.. University Of Abuja; NigeriaFil: Zenner, Lionel. Centre National de la Recherche Scientifique; FranciaFil: Vavre, Fabrice. Centre National de la Recherche Scientifique; FranciaFil: Chevillon, Christine. Centre National de la Recherche Scientifique; FranciaWiley Blackwell Publishing, Inc2017-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/58622Duron, Olivier; Binetruy, Florian; Noël, Valérie; Cremaschi, Julie; McCoy, Karen D.; et al.; Evolutionary changes in symbiont community structure in ticks; Wiley Blackwell Publishing, Inc; Molecular Ecology; 26; 11; 6-2017; 2905-29210962-1083CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1111/mec.14094info:eu-repo/semantics/altIdentifier/url/https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14094info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:06:15Zoai:ri.conicet.gov.ar:11336/58622instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-10 13:06:15.704CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Evolutionary changes in symbiont community structure in ticks
title Evolutionary changes in symbiont community structure in ticks
spellingShingle Evolutionary changes in symbiont community structure in ticks
Duron, Olivier
Co-Evolution
Heritable Symbiont Communities
Maternally Inherited Bacteria
Symbiosis
Tick
title_short Evolutionary changes in symbiont community structure in ticks
title_full Evolutionary changes in symbiont community structure in ticks
title_fullStr Evolutionary changes in symbiont community structure in ticks
title_full_unstemmed Evolutionary changes in symbiont community structure in ticks
title_sort Evolutionary changes in symbiont community structure in ticks
dc.creator.none.fl_str_mv Duron, Olivier
Binetruy, Florian
Noël, Valérie
Cremaschi, Julie
McCoy, Karen D.
Arnathau, Céline
Plantard, Olivier
Goolsby, John
Pérez de León, Adalberto A.
Heylen, Dieter J. A.
Van Oosten, A. Raoul
Gottlieb, Yuval
Baneth, Gad
Guglielmone, Alberto Alejandro
Estrada Peña, Agustin
Opara, Maxwell N.
Zenner, Lionel
Vavre, Fabrice
Chevillon, Christine
author Duron, Olivier
author_facet Duron, Olivier
Binetruy, Florian
Noël, Valérie
Cremaschi, Julie
McCoy, Karen D.
Arnathau, Céline
Plantard, Olivier
Goolsby, John
Pérez de León, Adalberto A.
Heylen, Dieter J. A.
Van Oosten, A. Raoul
Gottlieb, Yuval
Baneth, Gad
Guglielmone, Alberto Alejandro
Estrada Peña, Agustin
Opara, Maxwell N.
Zenner, Lionel
Vavre, Fabrice
Chevillon, Christine
author_role author
author2 Binetruy, Florian
Noël, Valérie
Cremaschi, Julie
McCoy, Karen D.
Arnathau, Céline
Plantard, Olivier
Goolsby, John
Pérez de León, Adalberto A.
Heylen, Dieter J. A.
Van Oosten, A. Raoul
Gottlieb, Yuval
Baneth, Gad
Guglielmone, Alberto Alejandro
Estrada Peña, Agustin
Opara, Maxwell N.
Zenner, Lionel
Vavre, Fabrice
Chevillon, Christine
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Co-Evolution
Heritable Symbiont Communities
Maternally Inherited Bacteria
Symbiosis
Tick
topic Co-Evolution
Heritable Symbiont Communities
Maternally Inherited Bacteria
Symbiosis
Tick
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Ecological specialization to restricted diet niches is driven by obligate, and often maternally inherited, symbionts in many arthropod lineages. These heritable symbionts typically form evolutionarily stable associations with arthropods that can last for millions of years. Ticks were recently found to harbour such an obligate symbiont, Coxiella-LE, that synthesizes B vitamins and cofactors not obtained in sufficient quantities from blood diet. In this study, the examination of 81 tick species shows that some Coxiella-LE symbioses are evolutionarily stable with an ancient acquisition followed by codiversification as observed in ticks belonging to the Rhipicephalus genus. However, many other Coxiella-LE symbioses are characterized by low evolutionary stability with frequent host shifts and extinction events. Further examination revealed the presence of nine other genera of maternally inherited bacteria in ticks. Although these nine symbionts were primarily thought to be facultative, their distribution among tick species rather suggests that at least four may have independently replaced Coxiella-LE and likely represent alternative obligate symbionts. Phylogenetic evidence otherwise indicates that cocladogenesis is globally rare in these symbioses as most originate via horizontal transfer of an existing symbiont between unrelated tick species. As a result, the structure of these symbiont communities is not fixed and stable across the tick phylogeny. Most importantly, the symbiont communities commonly reach high levels of diversity with up to six unrelated maternally inherited bacteria coexisting within host species. We further conjecture that interactions among coexisting symbionts are pivotal drivers of community structure both among and within tick species.
Fil: Duron, Olivier. Centre National de la Recherche Scientifique; Francia
Fil: Binetruy, Florian. Centre National de la Recherche Scientifique; Francia
Fil: Noël, Valérie. Centre National de la Recherche Scientifique; Francia
Fil: Cremaschi, Julie. Centre National de la Recherche Scientifique; Francia
Fil: McCoy, Karen D.. Centre National de la Recherche Scientifique; Francia
Fil: Arnathau, Céline. Centre National de la Recherche Scientifique; Francia
Fil: Plantard, Olivier. Institut National de la Recherche Agronomique; Francia
Fil: Goolsby, John. United States Department of Agriculture. Agriculture Research Service; Estados Unidos
Fil: Pérez de León, Adalberto A.. Veterinary Pest Genomics Center; Estados Unidos
Fil: Heylen, Dieter J. A.. Universiteit Antwerp; Bélgica
Fil: Van Oosten, A. Raoul. Universiteit Antwerp; Bélgica
Fil: Gottlieb, Yuval. The Hebrew University of Jerusalem; Israel
Fil: Baneth, Gad. The Hebrew University of Jerusalem; Israel
Fil: Guglielmone, Alberto Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Regional Buenos Aires; Argentina
Fil: Estrada Peña, Agustin. Universidad de Zaragoza; España
Fil: Opara, Maxwell N.. University Of Abuja; Nigeria
Fil: Zenner, Lionel. Centre National de la Recherche Scientifique; Francia
Fil: Vavre, Fabrice. Centre National de la Recherche Scientifique; Francia
Fil: Chevillon, Christine. Centre National de la Recherche Scientifique; Francia
description Ecological specialization to restricted diet niches is driven by obligate, and often maternally inherited, symbionts in many arthropod lineages. These heritable symbionts typically form evolutionarily stable associations with arthropods that can last for millions of years. Ticks were recently found to harbour such an obligate symbiont, Coxiella-LE, that synthesizes B vitamins and cofactors not obtained in sufficient quantities from blood diet. In this study, the examination of 81 tick species shows that some Coxiella-LE symbioses are evolutionarily stable with an ancient acquisition followed by codiversification as observed in ticks belonging to the Rhipicephalus genus. However, many other Coxiella-LE symbioses are characterized by low evolutionary stability with frequent host shifts and extinction events. Further examination revealed the presence of nine other genera of maternally inherited bacteria in ticks. Although these nine symbionts were primarily thought to be facultative, their distribution among tick species rather suggests that at least four may have independently replaced Coxiella-LE and likely represent alternative obligate symbionts. Phylogenetic evidence otherwise indicates that cocladogenesis is globally rare in these symbioses as most originate via horizontal transfer of an existing symbiont between unrelated tick species. As a result, the structure of these symbiont communities is not fixed and stable across the tick phylogeny. Most importantly, the symbiont communities commonly reach high levels of diversity with up to six unrelated maternally inherited bacteria coexisting within host species. We further conjecture that interactions among coexisting symbionts are pivotal drivers of community structure both among and within tick species.
publishDate 2017
dc.date.none.fl_str_mv 2017-06
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/58622
Duron, Olivier; Binetruy, Florian; Noël, Valérie; Cremaschi, Julie; McCoy, Karen D.; et al.; Evolutionary changes in symbiont community structure in ticks; Wiley Blackwell Publishing, Inc; Molecular Ecology; 26; 11; 6-2017; 2905-2921
0962-1083
CONICET Digital
CONICET
url http://hdl.handle.net/11336/58622
identifier_str_mv Duron, Olivier; Binetruy, Florian; Noël, Valérie; Cremaschi, Julie; McCoy, Karen D.; et al.; Evolutionary changes in symbiont community structure in ticks; Wiley Blackwell Publishing, Inc; Molecular Ecology; 26; 11; 6-2017; 2905-2921
0962-1083
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1111/mec.14094
info:eu-repo/semantics/altIdentifier/url/https://onlinelibrary.wiley.com/doi/abs/10.1111/mec.14094
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
_version_ 1842980254051729408
score 12.993085