Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas

Autores
Lukasik, Piotr; Nazario, Katherine; Van Leuven, James T.; Campbell, Matthew A.; Meyer, Mariah; Michalik, Anna; Pessacq, Pablo; Simon, Chris; Veloso, Claudio; McCutcheon, John P.
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Bacterial endosymbionts that provide nutrients to hosts often have genomes that are extremely stable in structure and gene content. In contrast, the genome of the endosymbiont Hodgkinia cicadicola has fractured into multiple distinct lineages in some species of the cicada genus Tettigades. To better understand the frequency, timing, and outcomes of Hodgkinia lineage splitting throughout this cicada genus, we sampled cicadas over three field seasons in Chile and performed genomics and microscopy on representative samples. We found that a single ancestral Hodgkinia lineage has split at least six independent times in Tettigades over the last 4 million years, resulting in complexes of between two and six distinct Hodgkinia lineages per host. Individual genomes in these symbiotic complexes differ dramatically in relative abundance, genome size, organization, and gene content. Each Hodgkinia lineage retains a small set of core genes involved in genetic information processing, but the high level of gene loss experienced by all genomes suggests that extensive sharing of gene products among symbiont cells must occur. In total, Hodgkinia complexes that consist of multiple lineages encode nearly complete sets of genes present on the ancestral single lineage and presumably perform the same functions as symbionts that have not undergone splitting. However, differences in the timing of the splits, along with dissimilar gene loss patterns on the resulting genomes, have led to very different outcomes of lineage splitting in extant cicadas.
Fil: Lukasik, Piotr. University of Montana; Estados Unidos
Fil: Nazario, Katherine. University of Connecticut; Estados Unidos
Fil: Van Leuven, James T.. University of Montana; Estados Unidos
Fil: Campbell, Matthew A.. University of Montana; Estados Unidos
Fil: Meyer, Mariah. University of Montana; Estados Unidos
Fil: Michalik, Anna. Jagiellonian University; Polonia
Fil: Pessacq, Pablo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Centro de Investigación Esquel de Montaña y Estepa Patagóica. Universidad Nacional de la Patagonia "San Juan Bosco". Facultad de Ciencias Naturales - Sede Esquel. Centro de Investigación Esquel de Montaña y Estepa Patagónica; Argentina
Fil: Simon, Chris. University of Connecticut; Estados Unidos
Fil: Veloso, Claudio. Universidad de Chile; Chile
Fil: McCutcheon, John P.. University of Montana; Estados Unidos
Materia
Cicadas
Genome Evolution
Mitochondria
Nutritional Endosymbiont
Organelle
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:11336/56661
Acceder
id CONICETDig_e67c2646d94496256a66e92046631a5a
oai_identifier_str oai:ri.conicet.gov.ar:11336/56661
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Multiple origins of interdependent endosymbiotic complexes in a genus of cicadasLukasik, PiotrNazario, KatherineVan Leuven, James T.Campbell, Matthew A.Meyer, MariahMichalik, AnnaPessacq, PabloSimon, ChrisVeloso, ClaudioMcCutcheon, John P.CicadasGenome EvolutionMitochondriaNutritional EndosymbiontOrganellehttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Bacterial endosymbionts that provide nutrients to hosts often have genomes that are extremely stable in structure and gene content. In contrast, the genome of the endosymbiont Hodgkinia cicadicola has fractured into multiple distinct lineages in some species of the cicada genus Tettigades. To better understand the frequency, timing, and outcomes of Hodgkinia lineage splitting throughout this cicada genus, we sampled cicadas over three field seasons in Chile and performed genomics and microscopy on representative samples. We found that a single ancestral Hodgkinia lineage has split at least six independent times in Tettigades over the last 4 million years, resulting in complexes of between two and six distinct Hodgkinia lineages per host. Individual genomes in these symbiotic complexes differ dramatically in relative abundance, genome size, organization, and gene content. Each Hodgkinia lineage retains a small set of core genes involved in genetic information processing, but the high level of gene loss experienced by all genomes suggests that extensive sharing of gene products among symbiont cells must occur. In total, Hodgkinia complexes that consist of multiple lineages encode nearly complete sets of genes present on the ancestral single lineage and presumably perform the same functions as symbionts that have not undergone splitting. However, differences in the timing of the splits, along with dissimilar gene loss patterns on the resulting genomes, have led to very different outcomes of lineage splitting in extant cicadas.Fil: Lukasik, Piotr. University of Montana; Estados UnidosFil: Nazario, Katherine. University of Connecticut; Estados UnidosFil: Van Leuven, James T.. University of Montana; Estados UnidosFil: Campbell, Matthew A.. University of Montana; Estados UnidosFil: Meyer, Mariah. University of Montana; Estados UnidosFil: Michalik, Anna. Jagiellonian University; PoloniaFil: Pessacq, Pablo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Centro de Investigación Esquel de Montaña y Estepa Patagóica. Universidad Nacional de la Patagonia "San Juan Bosco". Facultad de Ciencias Naturales - Sede Esquel. Centro de Investigación Esquel de Montaña y Estepa Patagónica; ArgentinaFil: Simon, Chris. University of Connecticut; Estados UnidosFil: Veloso, Claudio. Universidad de Chile; ChileFil: McCutcheon, John P.. University of Montana; Estados UnidosNational Academy of Sciences2017-01info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/56661Lukasik, Piotr; Nazario, Katherine; Van Leuven, James T.; Campbell, Matthew A.; Meyer, Mariah; et al.; Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 115; 2; 1-2017; E226-E2350027-8424CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.1712321115info:eu-repo/semantics/altIdentifier/url/http://www.pnas.org/content/115/2/E226info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:31:43Zoai:ri.conicet.gov.ar:11336/56661instacron: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:34982025-10-15 14:31:43.571CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas
title Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas
spellingShingle Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas
Lukasik, Piotr
Cicadas
Genome Evolution
Mitochondria
Nutritional Endosymbiont
Organelle
title_short Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas
title_full Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas
title_fullStr Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas
title_full_unstemmed Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas
title_sort Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas
dc.creator.none.fl_str_mv Lukasik, Piotr
Nazario, Katherine
Van Leuven, James T.
Campbell, Matthew A.
Meyer, Mariah
Michalik, Anna
Pessacq, Pablo
Simon, Chris
Veloso, Claudio
McCutcheon, John P.
author Lukasik, Piotr
author_facet Lukasik, Piotr
Nazario, Katherine
Van Leuven, James T.
Campbell, Matthew A.
Meyer, Mariah
Michalik, Anna
Pessacq, Pablo
Simon, Chris
Veloso, Claudio
McCutcheon, John P.
author_role author
author2 Nazario, Katherine
Van Leuven, James T.
Campbell, Matthew A.
Meyer, Mariah
Michalik, Anna
Pessacq, Pablo
Simon, Chris
Veloso, Claudio
McCutcheon, John P.
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Cicadas
Genome Evolution
Mitochondria
Nutritional Endosymbiont
Organelle
topic Cicadas
Genome Evolution
Mitochondria
Nutritional Endosymbiont
Organelle
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Bacterial endosymbionts that provide nutrients to hosts often have genomes that are extremely stable in structure and gene content. In contrast, the genome of the endosymbiont Hodgkinia cicadicola has fractured into multiple distinct lineages in some species of the cicada genus Tettigades. To better understand the frequency, timing, and outcomes of Hodgkinia lineage splitting throughout this cicada genus, we sampled cicadas over three field seasons in Chile and performed genomics and microscopy on representative samples. We found that a single ancestral Hodgkinia lineage has split at least six independent times in Tettigades over the last 4 million years, resulting in complexes of between two and six distinct Hodgkinia lineages per host. Individual genomes in these symbiotic complexes differ dramatically in relative abundance, genome size, organization, and gene content. Each Hodgkinia lineage retains a small set of core genes involved in genetic information processing, but the high level of gene loss experienced by all genomes suggests that extensive sharing of gene products among symbiont cells must occur. In total, Hodgkinia complexes that consist of multiple lineages encode nearly complete sets of genes present on the ancestral single lineage and presumably perform the same functions as symbionts that have not undergone splitting. However, differences in the timing of the splits, along with dissimilar gene loss patterns on the resulting genomes, have led to very different outcomes of lineage splitting in extant cicadas.
Fil: Lukasik, Piotr. University of Montana; Estados Unidos
Fil: Nazario, Katherine. University of Connecticut; Estados Unidos
Fil: Van Leuven, James T.. University of Montana; Estados Unidos
Fil: Campbell, Matthew A.. University of Montana; Estados Unidos
Fil: Meyer, Mariah. University of Montana; Estados Unidos
Fil: Michalik, Anna. Jagiellonian University; Polonia
Fil: Pessacq, Pablo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Centro de Investigación Esquel de Montaña y Estepa Patagóica. Universidad Nacional de la Patagonia "San Juan Bosco". Facultad de Ciencias Naturales - Sede Esquel. Centro de Investigación Esquel de Montaña y Estepa Patagónica; Argentina
Fil: Simon, Chris. University of Connecticut; Estados Unidos
Fil: Veloso, Claudio. Universidad de Chile; Chile
Fil: McCutcheon, John P.. University of Montana; Estados Unidos
description Bacterial endosymbionts that provide nutrients to hosts often have genomes that are extremely stable in structure and gene content. In contrast, the genome of the endosymbiont Hodgkinia cicadicola has fractured into multiple distinct lineages in some species of the cicada genus Tettigades. To better understand the frequency, timing, and outcomes of Hodgkinia lineage splitting throughout this cicada genus, we sampled cicadas over three field seasons in Chile and performed genomics and microscopy on representative samples. We found that a single ancestral Hodgkinia lineage has split at least six independent times in Tettigades over the last 4 million years, resulting in complexes of between two and six distinct Hodgkinia lineages per host. Individual genomes in these symbiotic complexes differ dramatically in relative abundance, genome size, organization, and gene content. Each Hodgkinia lineage retains a small set of core genes involved in genetic information processing, but the high level of gene loss experienced by all genomes suggests that extensive sharing of gene products among symbiont cells must occur. In total, Hodgkinia complexes that consist of multiple lineages encode nearly complete sets of genes present on the ancestral single lineage and presumably perform the same functions as symbionts that have not undergone splitting. However, differences in the timing of the splits, along with dissimilar gene loss patterns on the resulting genomes, have led to very different outcomes of lineage splitting in extant cicadas.
publishDate 2017
dc.date.none.fl_str_mv 2017-01
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/11336/56661
Lukasik, Piotr; Nazario, Katherine; Van Leuven, James T.; Campbell, Matthew A.; Meyer, Mariah; et al.; Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 115; 2; 1-2017; E226-E235
0027-8424
CONICET Digital
CONICET
url http://hdl.handle.net/11336/56661
identifier_str_mv Lukasik, Piotr; Nazario, Katherine; Van Leuven, James T.; Campbell, Matthew A.; Meyer, Mariah; et al.; Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 115; 2; 1-2017; E226-E235
0027-8424
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.1712321115
info:eu-repo/semantics/altIdentifier/url/http://www.pnas.org/content/115/2/E226
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 National Academy of Sciences
publisher.none.fl_str_mv National Academy of Sciences
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_ 1846082802685050880
score 13.221938

Publicaciones similares