Natural Selection for operons depends on genome size

Autores
Nuñez, Pablo Alfredo; Hector, Romero; Farber, Marisa Diana; Rocha, Eduardo
Año de publicación
2013
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
In prokaryotes, genome size is associated with metabolic versatility, regulatory complexity, effective population size and horizontal transfer rates. We therefore analyzed the co-variation of genome size and operon conservation to assess the evolutionary models of operon formation and maintenance. In agreement with previous results, intra-operonic pairs of essential and of highly expressed genes are more conserved. Interestingly, intra-operonic pairs of genes are also more conserved when they encode proteins at similar cell concentrations, suggesting a role of co-transcription in diminishing the cost of waste and shortfall in gene expression. Larger genomes have fewer and smaller operons that are also less conserved. Importantly, lower conservation in larger genomes was observed for all classes of operons in terms of gene expression, essentiality and balanced protein concentration. We reached very similar conclusions in independent analyses of three major bacterial clades (α- and β-Proteobacteria and Firmicutes). Operon conservation is inversely correlated to the abundance of transcription factors in the genome when controlled for genome size. This suggests a negative association between the complexity of genetic networks and operon conservation. These results show that genome size and/or its proxies are key determinants of the intensity of natural selection for operon organization. Our data fits better the evolutionary models based on the advantage of co-regulation than those based on genetic linkage or stochastic gene expression. We suggest that larger genomes with highly complex genetic networks and many transcription factors endure weaker selection for operons than smaller genomes with fewer alternative tools for genetic regulation.
Fil: Nuñez, Pablo Alfredo. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias. Centro de Investigación de Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Hector, Romero. Universidad de la Republica; Uruguay
Fil: Farber, Marisa Diana. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias. Centro de Investigación de Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Rocha, Eduardo. Instituto Pasteur; Francia
Materia
Operons
Prokaryotes
Evolution
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:11336/9011
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/9011
network_acronym_str CONICETDig
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network_name_str CONICET Digital (CONICET)
spelling Natural Selection for operons depends on genome sizeNuñez, Pablo AlfredoHector, RomeroFarber, Marisa DianaRocha, EduardoOperonsProkaryotesEvolutionhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1In prokaryotes, genome size is associated with metabolic versatility, regulatory complexity, effective population size and horizontal transfer rates. We therefore analyzed the co-variation of genome size and operon conservation to assess the evolutionary models of operon formation and maintenance. In agreement with previous results, intra-operonic pairs of essential and of highly expressed genes are more conserved. Interestingly, intra-operonic pairs of genes are also more conserved when they encode proteins at similar cell concentrations, suggesting a role of co-transcription in diminishing the cost of waste and shortfall in gene expression. Larger genomes have fewer and smaller operons that are also less conserved. Importantly, lower conservation in larger genomes was observed for all classes of operons in terms of gene expression, essentiality and balanced protein concentration. We reached very similar conclusions in independent analyses of three major bacterial clades (α- and β-Proteobacteria and Firmicutes). Operon conservation is inversely correlated to the abundance of transcription factors in the genome when controlled for genome size. This suggests a negative association between the complexity of genetic networks and operon conservation. These results show that genome size and/or its proxies are key determinants of the intensity of natural selection for operon organization. Our data fits better the evolutionary models based on the advantage of co-regulation than those based on genetic linkage or stochastic gene expression. We suggest that larger genomes with highly complex genetic networks and many transcription factors endure weaker selection for operons than smaller genomes with fewer alternative tools for genetic regulation.Fil: Nuñez, Pablo Alfredo. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias. Centro de Investigación de Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Hector, Romero. Universidad de la Republica; UruguayFil: Farber, Marisa Diana. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias. Centro de Investigación de Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Rocha, Eduardo. Instituto Pasteur; FranciaOxford University Press2013-11info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/9011Nuñez, Pablo Alfredo; Hector, Romero; Farber, Marisa Diana; Rocha, Eduardo; Natural Selection for operons depends on genome size; Oxford University Press; Genome Biology and Evolution; 5; 11; 11-2013; 2242-22541759-6653enginfo:eu-repo/semantics/altIdentifier/url/http://gbe.oxfordjournals.org/content/5/11/2242info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3845653/info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:39:51Zoai:ri.conicet.gov.ar:11336/9011instacron: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:34982025-09-29 09:39:52.004CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Natural Selection for operons depends on genome size
title Natural Selection for operons depends on genome size
spellingShingle Natural Selection for operons depends on genome size
Nuñez, Pablo Alfredo
Operons
Prokaryotes
Evolution
title_short Natural Selection for operons depends on genome size
title_full Natural Selection for operons depends on genome size
title_fullStr Natural Selection for operons depends on genome size
title_full_unstemmed Natural Selection for operons depends on genome size
title_sort Natural Selection for operons depends on genome size
dc.creator.none.fl_str_mv Nuñez, Pablo Alfredo
Hector, Romero
Farber, Marisa Diana
Rocha, Eduardo
author Nuñez, Pablo Alfredo
author_facet Nuñez, Pablo Alfredo
Hector, Romero
Farber, Marisa Diana
Rocha, Eduardo
author_role author
author2 Hector, Romero
Farber, Marisa Diana
Rocha, Eduardo
author2_role author
author
author
dc.subject.none.fl_str_mv Operons
Prokaryotes
Evolution
topic Operons
Prokaryotes
Evolution
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv In prokaryotes, genome size is associated with metabolic versatility, regulatory complexity, effective population size and horizontal transfer rates. We therefore analyzed the co-variation of genome size and operon conservation to assess the evolutionary models of operon formation and maintenance. In agreement with previous results, intra-operonic pairs of essential and of highly expressed genes are more conserved. Interestingly, intra-operonic pairs of genes are also more conserved when they encode proteins at similar cell concentrations, suggesting a role of co-transcription in diminishing the cost of waste and shortfall in gene expression. Larger genomes have fewer and smaller operons that are also less conserved. Importantly, lower conservation in larger genomes was observed for all classes of operons in terms of gene expression, essentiality and balanced protein concentration. We reached very similar conclusions in independent analyses of three major bacterial clades (α- and β-Proteobacteria and Firmicutes). Operon conservation is inversely correlated to the abundance of transcription factors in the genome when controlled for genome size. This suggests a negative association between the complexity of genetic networks and operon conservation. These results show that genome size and/or its proxies are key determinants of the intensity of natural selection for operon organization. Our data fits better the evolutionary models based on the advantage of co-regulation than those based on genetic linkage or stochastic gene expression. We suggest that larger genomes with highly complex genetic networks and many transcription factors endure weaker selection for operons than smaller genomes with fewer alternative tools for genetic regulation.
Fil: Nuñez, Pablo Alfredo. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias. Centro de Investigación de Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Hector, Romero. Universidad de la Republica; Uruguay
Fil: Farber, Marisa Diana. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias. Centro de Investigación de Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Rocha, Eduardo. Instituto Pasteur; Francia
description In prokaryotes, genome size is associated with metabolic versatility, regulatory complexity, effective population size and horizontal transfer rates. We therefore analyzed the co-variation of genome size and operon conservation to assess the evolutionary models of operon formation and maintenance. In agreement with previous results, intra-operonic pairs of essential and of highly expressed genes are more conserved. Interestingly, intra-operonic pairs of genes are also more conserved when they encode proteins at similar cell concentrations, suggesting a role of co-transcription in diminishing the cost of waste and shortfall in gene expression. Larger genomes have fewer and smaller operons that are also less conserved. Importantly, lower conservation in larger genomes was observed for all classes of operons in terms of gene expression, essentiality and balanced protein concentration. We reached very similar conclusions in independent analyses of three major bacterial clades (α- and β-Proteobacteria and Firmicutes). Operon conservation is inversely correlated to the abundance of transcription factors in the genome when controlled for genome size. This suggests a negative association between the complexity of genetic networks and operon conservation. These results show that genome size and/or its proxies are key determinants of the intensity of natural selection for operon organization. Our data fits better the evolutionary models based on the advantage of co-regulation than those based on genetic linkage or stochastic gene expression. We suggest that larger genomes with highly complex genetic networks and many transcription factors endure weaker selection for operons than smaller genomes with fewer alternative tools for genetic regulation.
publishDate 2013
dc.date.none.fl_str_mv 2013-11
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/11336/9011
Nuñez, Pablo Alfredo; Hector, Romero; Farber, Marisa Diana; Rocha, Eduardo; Natural Selection for operons depends on genome size; Oxford University Press; Genome Biology and Evolution; 5; 11; 11-2013; 2242-2254
1759-6653
url http://hdl.handle.net/11336/9011
identifier_str_mv Nuñez, Pablo Alfredo; Hector, Romero; Farber, Marisa Diana; Rocha, Eduardo; Natural Selection for operons depends on genome size; Oxford University Press; Genome Biology and Evolution; 5; 11; 11-2013; 2242-2254
1759-6653
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://gbe.oxfordjournals.org/content/5/11/2242
info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3845653/
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
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
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
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score 13.069144

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