title: Characterization of Function of the GlgA2 Glycogen/Starch Synthase in Cyanobacterium sp. Clg1 Highlights Convergent Evolution of Glycogen Metabolism into Starch Granule Aggregation.
abstract: At variance with the starch-accumulating plants and most of the glycogen-accumulating cyanobacteria, Cyanobacterium sp. CLg1 synthesizes both glycogen and starch. We now report the selection of a starchless mutant of this cyanobacterium that retains wild-type amounts of glycogen. Unlike other mutants of this type found in plants and cyanobacteria, this mutant proved to be selectively defective for one of the two types of glycogen/starch synthase: GlgA2. This enzyme is phylogenetically related to the previously reported SSIII/SSIV starch synthase that is thought to be involved in starch granule seeding in plants. This suggests that, in addition to the selective polysaccharide debranching demonstrated to be responsible for starch rather than glycogen synthesis, the nature and properties of the elongation enzyme define a novel determinant of starch versus glycogen accumulation. We show that the phylogenies of GlgA2 and of 16S ribosomal RNA display significant congruence. This suggests that this enzyme evolved together with cyanobacteria when they diversified over 2 billion years ago. However, cyanobacteria can be ruled out as direct progenitors of the SSIII/SSIV ancestral gene found in Archaeplastida. Hence, both cyanobacteria and plants recruited similar enzymes independently to perform analogous tasks, further emphasizing the importance of convergent evolution in the appearance of starch from a preexisting glycogen metabolism network.
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Derifa
authors.initials: D
authors.lastname: Kadouche
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Mathieu
authors.identifier: 0000-0003-4941-4266
authors.initials: M
authors.lastname: Ducatez
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Ugo
authors.identifier: 0000-0001-9725-9833
authors.initials: U
authors.lastname: Cenci
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Catherine
authors.identifier: 0000-0002-0424-5828
authors.initials: C
authors.lastname: Tirtiaux
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Eiji
authors.identifier: 0000-0002-0153-7497
authors.initials: E
authors.lastname: Suzuki
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Yasunori
authors.identifier: 0000-0001-7660-0078
authors.initials: Y
authors.lastname: Nakamura
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Jean-Luc
authors.identifier: 0000-0002-9760-5369
authors.initials: JL
authors.lastname: Putaux
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Amandine Durand
authors.identifier: 0000-0003-3415-1512
authors.initials: AD
authors.lastname: Terrasson
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Sandra
authors.identifier: 0000-0002-5878-9062
authors.initials: S
authors.lastname: Diaz-Troya
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Francisco Javier
authors.identifier: 0000-0002-2068-7861
authors.initials: FJ
authors.lastname: Florencio
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Maria Cecilia
authors.initials: MC
authors.lastname: Arias
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Alexander
authors.identifier: 0000-0002-0910-2885
authors.initials: A
authors.lastname: Striebeck
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.).
authors.forename: Monica
authors.identifier: 0000-0002-5221-089X
authors.initials: M
authors.lastname: Palcic
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.) steven.ball@univ-lille1.fr christophe.colleoni@univ-lille1.fr.
authors.forename: Steven G
authors.identifier: 0000-0003-1629-1650
authors.initials: SG
authors.lastname: Ball
authors.affiliation: Université Lille, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Unité Mixte de Recherche 8576, Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France (D.K., M.D., U.C., C.T., M.C.A., S.G.B., C.C.);Department of Biological Production, Akita Prefectural University, Akita 010-0195 Japan (E.S., Y.N.);Centre de Recherches sur Les Macromolécules Végétales, Centre National de la Recherche Scientifique, Université Grenoble Alpes, F-38041 Grenoble cedex 9, France (J.-L.P., A.D.T.);Instituto de Bioquímica Vegetal y Fotosíntesis cic Cartuja, Consejo Superior de Investigaciones Científicas-Universidad de Sevilla, 41092 Seville, Spain (S.D.-T., F.J.F.);Raw Materials Group, Carlsberg Laboratory, 1799 Copenhagen V, Denmark (A.S.); andDepartment of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6 (M.P.) steven.ball@univ-lille1.fr christophe.colleoni@univ-lille1.fr.
authors.forename: Christophe
authors.identifier: 0000-0002-6534-6120
authors.initials: C
authors.lastname: Colleoni
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D005075:Biological Evolution; D000458:Cyanobacteria / Q000378:metabolism* / Q000502:physiology; D004926:Escherichia coli / Q000235:genetics / Q000378:metabolism; D016680:Genome, Bacterial; D006003:Glycogen / Q000737:chemistry / Q000378:metabolism*; D006006:Glycogen Synthase / Q000235:genetics / Q000378:metabolism; D009154:Mutation; D010802:Phylogeny; D011135:Polysaccharides, Bacterial / Q000235:genetics / Q000378:metabolism; D013213:Starch / Q000378:metabolism; D013214:Starch Synthase / Q000235:genetics / Q000378:metabolism*; D046939:Synechocystis / Q000235:genetics / Q000378:metabolism
chemical_list: D001426:Bacterial Proteins; D011135:Polysaccharides, Bacterial; D013213:Starch; D006003:Glycogen; D006006:Glycogen Synthase; D013214:Starch Synthase