title: Operon structure and cotranslational subunit association direct protein assembly in bacteria.
abstract: Assembly of protein complexes is considered a posttranslational process involving random collision of subunits. We show that within the Escherichia coli cytosol, bacterial luciferase subunits LuxA and LuxB assemble into complexes close to the site of subunit synthesis. Assembly efficiency decreases markedly if subunits are synthesized on separate messenger RNAs from genes integrated at distant chromosomal sites. Subunit assembly initiates cotranslationally on nascent LuxB in vivo. The ribosome-associated chaperone trigger factor delays the onset of cotranslational interactions until the LuxB dimer interface is fully exposed. Protein assembly is thus directly coupled to the translation process and involves spatially confined, actively chaperoned cotranslational subunit interactions. Bacterial gene organization into operons therefore reflects a fundamental cotranslational mechanism for spatial and temporal regulation that is vital to effective assembly of protein complexes.
authors.affiliation: Center for Molecular Biology of the University of Heidelberg (ZMBH) and German Cancer Research Center (DKFZ), DKFZ-ZMBH Alliance, Im Neuenheimer Feld 282, Heidelberg D-69120, Germany.
authors.forename: Yu-Wei
authors.initials: YW
authors.lastname: Shieh
authors.affiliation: European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, 69117 Heidelberg, Germany.
authors.forename: Pablo
authors.initials: P
authors.lastname: Minguez
authors.affiliation: European Molecular Biology Laboratory (EMBL), Meyerhofstrasse 1, 69117 Heidelberg, Germany. Max-Delbrück-Centre for Molecular Medicine, Robert-Rössle-Strasse 10, 13125 Berlin, Germany.
authors.forename: Peer
authors.initials: P
authors.lastname: Bork
authors.affiliation: Center for Molecular Biology of the University of Heidelberg (ZMBH) and German Cancer Research Center (DKFZ), DKFZ-ZMBH Alliance, Im Neuenheimer Feld 282, Heidelberg D-69120, Germany.
authors.forename: Josef J
authors.initials: JJ
authors.lastname: Auburger
authors.affiliation: Center for Molecular Biology of the University of Heidelberg (ZMBH) and German Cancer Research Center (DKFZ), DKFZ-ZMBH Alliance, Im Neuenheimer Feld 282, Heidelberg D-69120, Germany. Malaria Research Foundation, Post Office Box 10420, Aspen, CO 81612, USA.
authors.forename: D Lys
authors.initials: DL
authors.lastname: Guilbride
authors.affiliation: Center for Molecular Biology of the University of Heidelberg (ZMBH) and German Cancer Research Center (DKFZ), DKFZ-ZMBH Alliance, Im Neuenheimer Feld 282, Heidelberg D-69120, Germany. bukau@zmbh.uni-heidelberg.de g.kramer@zmbh.uni-heidelberg.de.
authors.forename: Günter
authors.initials: G
authors.lastname: Kramer
authors.affiliation: Center for Molecular Biology of the University of Heidelberg (ZMBH) and German Cancer Research Center (DKFZ), DKFZ-ZMBH Alliance, Im Neuenheimer Feld 282, Heidelberg D-69120, Germany. bukau@zmbh.uni-heidelberg.de g.kramer@zmbh.uni-heidelberg.de.
authors.forename: Bernd
authors.initials: B
authors.lastname: Bukau
mesh_terms: D001419:Bacteria / Q000235:genetics* / Q000378:metabolism*; D001426:Bacterial Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D004926:Escherichia coli; D023061:Gene Order; D005798:Genes, Bacterial; D049452:Green Fluorescent Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D049453:Luciferases, Bacterial / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism*; D008164:Luminescent Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D018832:Molecular Chaperones / Q000378:metabolism; D009876:Operon; D014176:Protein Biosynthesis; D017433:Protein Structure, Secondary; D021122:Protein Subunits / Q000737:chemistry / Q000172:deficiency / Q000235:genetics / Q000378:metabolism; D012333:RNA, Messenger / Q000378:metabolism; D011993:Recombinant Fusion Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D012270:Ribosomes / Q000378:metabolism; D014733:Vibrio / Q000201:enzymology
chemical_list: D001426:Bacterial Proteins; C485182:Cyan Fluorescent Protein; D008164:Luminescent Proteins; D018832:Molecular Chaperones; D021122:Protein Subunits; D012333:RNA, Messenger; D011993:Recombinant Fusion Proteins; C054562:yellow fluorescent protein, Bacteria; D049452:Green Fluorescent Proteins; D049453:Luciferases, Bacterial