Comparative genomic and phylogenetic analyses of gammaproteobacterial glg genes traced the origin of the Escherichia coli glycogen glgBXCAP operon to the last common ancestor of the sister orders Enterobacteriales and Pasteurellales

© 2015 Almagro et al. Production of branched α-glucan, glycogen-like polymers is widely spread in the Bacteria domain. The glycogen pathway of synthesis and degradation has been fairly well characterized in the model enterobacterial species Escherichia coli (order Enterobacteriales, class Gammaprote...

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Autores: Almagro, Goizeder, Viale, Alejandro M., Montero, Manuel, Rahimpour, Mehdi, Muñoz Pérez, Francisco José, Baroja-Fernández, Edurne, Bahaji, Abdellatif, Zúñiga, Manuel, González-Candelas, Fernando, Pozueta-Romero, Javier
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2015
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/110636
Acceso en línea:http://hdl.handle.net/10261/110636
Access Level:acceso abierto
Palabra clave:glycogen
Amino acid sequence
Genome evolution
Bacterial evolution
Phylogenetic analysis
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spelling Comparative genomic and phylogenetic analyses of gammaproteobacterial glg genes traced the origin of the Escherichia coli glycogen glgBXCAP operon to the last common ancestor of the sister orders Enterobacteriales and PasteurellalesAlmagro, GoizederViale, Alejandro M.Montero, ManuelRahimpour, MehdiMuñoz Pérez, Francisco JoséBaroja-Fernández, EdurneBahaji, AbdellatifZúñiga, ManuelGonzález-Candelas, FernandoPozueta-Romero, JavierglycogenAmino acid sequenceGenome evolutionBacterial evolutionPhylogenetic analysis© 2015 Almagro et al. Production of branched α-glucan, glycogen-like polymers is widely spread in the Bacteria domain. The glycogen pathway of synthesis and degradation has been fairly well characterized in the model enterobacterial species Escherichia coli (order Enterobacteriales, class Gammaproteobacteria), in which the cognate genes (branching enzyme glgB, debranching enzyme glgX, ADP-glucose pyrophosphorylase glgC, glycogen synthase glgA, and glycogen phosphorylase glgP) are clustered in a glgBXCAP operon arrangement. However, the evolutionary origin of this particular arrangement and of its constituent genes is unknown. Here, by using 265 complete gammaproteobacterial genomes we have carried out a comparative analysis of the presence, copy number and arrangement of glg genes in all lineages of the Gammaproteobacteria. These analyses revealed large variations in glg gene presence, copy number and arrangements among different gammaproteobacterial lineages. However, the glgBXCAP arrangement was remarkably conserved in all glg-possessing species of the orders Enterobacteriales and Pasteurellales (the E/P group). Subsequent phylogenetic analyses of glg genes present in the Gammaproteobacteria and in other main bacterial groups indicated that glg genes have undergone a complex evolutionary history in which horizontal gene transfer may have played an important role. These analyses also revealed that the E/P glgBXCAP genes (a) share a common evolutionary origin, (b) were vertically transmitted within the E/P group, and (c) are closely related to glg genes of some phylogenetically distant betaproteobacterial species. The overall data allowed tracing the origin of the E. coli glgBXCAP operon to the last common ancestor of the E/P group, and also to uncover a likely glgBXCAP transfer event from the E/P group to particular lineages of the Betaproteobacteria.This research was partially supported by the grant [BIO2010-18239] from the Comisión Interministerial de Ciencia y Tecnología and Fondo Europeo de Desarrollo Regional (Spain). MR acknowledges a pre-doctoral JAE fellowship from the Consejo Superior de Investigaciones Científicas. AMV is grateful to the funding of the Programa Campus Iberus de Excelencia Internacional, Ministerio de Educación, Spain. His 2-month visit (January-March 2014) to the Institute of Agrobiotechnology, Public Universtity of Navarra, Pamplona, Spain, was included into the Proyecto financiado por el Ministerio de Educación en el marco del Programa Campus de Excelencia Internacional. FGC was supported by project [BFU2011-24112] from the Ministerio de Ciencia e Innovación (Spain).Peer ReviewedPublic Library of ScienceComisión Interministerial de Ciencia y Tecnología, CICYT (España)European CommissionConsejo Superior de Investigaciones Científicas (España)Ministerio de Ciencia e Innovación (España)Ministerio de Educación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2015201520152015info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/110636reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttp://doi.org/10.1371/journal.pone.0115516Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/1106362026-05-22T06:33:51Z
dc.title.none.fl_str_mv Comparative genomic and phylogenetic analyses of gammaproteobacterial glg genes traced the origin of the Escherichia coli glycogen glgBXCAP operon to the last common ancestor of the sister orders Enterobacteriales and Pasteurellales
title Comparative genomic and phylogenetic analyses of gammaproteobacterial glg genes traced the origin of the Escherichia coli glycogen glgBXCAP operon to the last common ancestor of the sister orders Enterobacteriales and Pasteurellales
spellingShingle Comparative genomic and phylogenetic analyses of gammaproteobacterial glg genes traced the origin of the Escherichia coli glycogen glgBXCAP operon to the last common ancestor of the sister orders Enterobacteriales and Pasteurellales
Almagro, Goizeder
glycogen
Amino acid sequence
Genome evolution
Bacterial evolution
Phylogenetic analysis
title_short Comparative genomic and phylogenetic analyses of gammaproteobacterial glg genes traced the origin of the Escherichia coli glycogen glgBXCAP operon to the last common ancestor of the sister orders Enterobacteriales and Pasteurellales
title_full Comparative genomic and phylogenetic analyses of gammaproteobacterial glg genes traced the origin of the Escherichia coli glycogen glgBXCAP operon to the last common ancestor of the sister orders Enterobacteriales and Pasteurellales
title_fullStr Comparative genomic and phylogenetic analyses of gammaproteobacterial glg genes traced the origin of the Escherichia coli glycogen glgBXCAP operon to the last common ancestor of the sister orders Enterobacteriales and Pasteurellales
title_full_unstemmed Comparative genomic and phylogenetic analyses of gammaproteobacterial glg genes traced the origin of the Escherichia coli glycogen glgBXCAP operon to the last common ancestor of the sister orders Enterobacteriales and Pasteurellales
title_sort Comparative genomic and phylogenetic analyses of gammaproteobacterial glg genes traced the origin of the Escherichia coli glycogen glgBXCAP operon to the last common ancestor of the sister orders Enterobacteriales and Pasteurellales
dc.creator.none.fl_str_mv Almagro, Goizeder
Viale, Alejandro M.
Montero, Manuel
Rahimpour, Mehdi
Muñoz Pérez, Francisco José
Baroja-Fernández, Edurne
Bahaji, Abdellatif
Zúñiga, Manuel
González-Candelas, Fernando
Pozueta-Romero, Javier
author Almagro, Goizeder
author_facet Almagro, Goizeder
Viale, Alejandro M.
Montero, Manuel
Rahimpour, Mehdi
Muñoz Pérez, Francisco José
Baroja-Fernández, Edurne
Bahaji, Abdellatif
Zúñiga, Manuel
González-Candelas, Fernando
Pozueta-Romero, Javier
author_role author
author2 Viale, Alejandro M.
Montero, Manuel
Rahimpour, Mehdi
Muñoz Pérez, Francisco José
Baroja-Fernández, Edurne
Bahaji, Abdellatif
Zúñiga, Manuel
González-Candelas, Fernando
Pozueta-Romero, Javier
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Comisión Interministerial de Ciencia y Tecnología, CICYT (España)
European Commission
Consejo Superior de Investigaciones Científicas (España)
Ministerio de Ciencia e Innovación (España)
Ministerio de Educación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv glycogen
Amino acid sequence
Genome evolution
Bacterial evolution
Phylogenetic analysis
topic glycogen
Amino acid sequence
Genome evolution
Bacterial evolution
Phylogenetic analysis
description © 2015 Almagro et al. Production of branched α-glucan, glycogen-like polymers is widely spread in the Bacteria domain. The glycogen pathway of synthesis and degradation has been fairly well characterized in the model enterobacterial species Escherichia coli (order Enterobacteriales, class Gammaproteobacteria), in which the cognate genes (branching enzyme glgB, debranching enzyme glgX, ADP-glucose pyrophosphorylase glgC, glycogen synthase glgA, and glycogen phosphorylase glgP) are clustered in a glgBXCAP operon arrangement. However, the evolutionary origin of this particular arrangement and of its constituent genes is unknown. Here, by using 265 complete gammaproteobacterial genomes we have carried out a comparative analysis of the presence, copy number and arrangement of glg genes in all lineages of the Gammaproteobacteria. These analyses revealed large variations in glg gene presence, copy number and arrangements among different gammaproteobacterial lineages. However, the glgBXCAP arrangement was remarkably conserved in all glg-possessing species of the orders Enterobacteriales and Pasteurellales (the E/P group). Subsequent phylogenetic analyses of glg genes present in the Gammaproteobacteria and in other main bacterial groups indicated that glg genes have undergone a complex evolutionary history in which horizontal gene transfer may have played an important role. These analyses also revealed that the E/P glgBXCAP genes (a) share a common evolutionary origin, (b) were vertically transmitted within the E/P group, and (c) are closely related to glg genes of some phylogenetically distant betaproteobacterial species. The overall data allowed tracing the origin of the E. coli glgBXCAP operon to the last common ancestor of the E/P group, and also to uncover a likely glgBXCAP transfer event from the E/P group to particular lineages of the Betaproteobacteria.
publishDate 2015
dc.date.none.fl_str_mv 2015
2015
2015
2015
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/110636
url http://hdl.handle.net/10261/110636
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv http://doi.org/10.1371/journal.pone.0115516
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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