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.
abstract: 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.
authors.affiliation: Instituto de Agrobiotecnología (CSIC/UPNA/Gobierno de Navarra), Iruñako etorbidea 123, 31192 Mutiloabeti, Nafarroa, Spain.
authors.forename: Goizeder
authors.initials: G
authors.lastname: Almagro
authors.affiliation: Instituto de Biología Molecular y Celular de Rosario (IBR, CONICET), Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario (UNR), Suipacha 531, 2000 Rosario, Argentina.
authors.forename: Alejandro M
authors.initials: AM
authors.lastname: Viale
authors.affiliation: Instituto de Agrobiotecnología (CSIC/UPNA/Gobierno de Navarra), Iruñako etorbidea 123, 31192 Mutiloabeti, Nafarroa, Spain.
authors.forename: Manuel
authors.initials: M
authors.lastname: Montero
authors.affiliation: Instituto de Agrobiotecnología (CSIC/UPNA/Gobierno de Navarra), Iruñako etorbidea 123, 31192 Mutiloabeti, Nafarroa, Spain.
authors.forename: Mehdi
authors.initials: M
authors.lastname: Rahimpour
authors.affiliation: Instituto de Agrobiotecnología (CSIC/UPNA/Gobierno de Navarra), Iruñako etorbidea 123, 31192 Mutiloabeti, Nafarroa, Spain.
authors.forename: Francisco José
authors.initials: FJ
authors.lastname: Muñoz
authors.affiliation: Instituto de Agrobiotecnología (CSIC/UPNA/Gobierno de Navarra), Iruñako etorbidea 123, 31192 Mutiloabeti, Nafarroa, Spain.
authors.forename: Edurne
authors.initials: E
authors.lastname: Baroja-Fernández
authors.affiliation: Instituto de Agrobiotecnología (CSIC/UPNA/Gobierno de Navarra), Iruñako etorbidea 123, 31192 Mutiloabeti, Nafarroa, Spain.
authors.forename: Abdellatif
authors.initials: A
authors.lastname: Bahaji
authors.affiliation: Dpt. Biotecnología de Alimentos, Instituto de Agroquímica y Tecnología de Alimentos, CSIC, Calle Agustín Escardino, 7, 46980 Paterna, Valencia, Spain.
authors.forename: Manuel
authors.initials: M
authors.lastname: Zúñiga
authors.affiliation: Unidad Mixta Genómica y Salud, FISABIO-Salud Pública/Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Universidad de Valencia, Calle Catedrático José Beltrán Martínez, 246980 Paterna, Valencia, Spain.
authors.forename: Fernando
authors.initials: F
authors.lastname: González-Candelas
authors.affiliation: Instituto de Agrobiotecnología (CSIC/UPNA/Gobierno de Navarra), Iruñako etorbidea 123, 31192 Mutiloabeti, Nafarroa, Spain.
authors.forename: Javier
authors.initials: J
authors.lastname: Pozueta-Romero
mesh_terms: D004926:Escherichia coli / Q000235:genetics*; D019143:Evolution, Molecular; D006003:Glycogen / Q000235:genetics*; D009876:Operon; D015661:Pasteurellaceae / Q000235:genetics*; D010802:Phylogeny
chemical_list: D006003:Glycogen