title: Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division.
abstract: To maintain cellular structure and integrity during division, Gram-negative bacteria must carefully coordinate constriction of a tripartite cell envelope of inner membrane, peptidoglycan (PG), and outer membrane (OM). It has remained enigmatic how this is accomplished. Here, we show that envelope machines facilitating septal PG synthesis (PBP1B-LpoB complex) and OM constriction (Tol system) are physically and functionally coordinated via YbgF, renamed CpoB (Coordinator of PG synthesis and OM constriction, associated with PBP1B). CpoB localizes to the septum concurrent with PBP1B-LpoB and Tol at the onset of constriction, interacts with both complexes, and regulates PBP1B activity in response to Tol energy state. This coordination links PG synthesis with OM invagination and imparts a unique mode of bifunctional PG synthase regulation by selectively modulating PBP1B cross-linking activity. Coordination of the PBP1B and Tol machines by CpoB contributes to effective PBP1B function in vivo and maintenance of cell envelope integrity during division.
authors.affiliation: Department of Microbiology and Immunology, University of California, San Francisco, San Francisco, United States.
authors.forename: Andrew N
authors.initials: AN
authors.lastname: Gray
authors.affiliation: Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle Upon Tyne, United Kingdom.
authors.forename: Alexander J F
authors.initials: AJ
authors.lastname: Egan
authors.affiliation: Membrane Biochemistry and Biophysics, Bijvoet Centre for Biomolecular Research, University of Utrecht, Utrecht, The Netherlands.
authors.forename: Inge L
authors.initials: IL
authors.lastname: Van't Veer
authors.affiliation: Bacterial Cell Biology, Swammerdam Institute for Life Sciences, Faculty of Science, University of Amsterdam, Amsterdam, The Netherlands.
authors.forename: Jolanda
authors.initials: J
authors.lastname: Verheul
authors.affiliation: Biophysics Program, Stanford University, Stanford, United States.
authors.forename: Alexandre
authors.initials: A
authors.lastname: Colavin
authors.affiliation: Genome Biology Unit, European Molecular Biology Laboratory Heidelberg, Heidelberg, Germany.
authors.forename: Alexandra
authors.identifier: http://orcid.org/0000-0001-8368-4193
authors.initials: A
authors.lastname: Koumoutsi
authors.affiliation: Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle Upon Tyne, United Kingdom.
authors.forename: Jacob
authors.initials: J
authors.lastname: Biboy
authors.affiliation: Biomolecular Mass Spectrometry and Proteomics, Bijvoet Centre for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, University of Utrecht, Utrecht, The Netherlands.
authors.forename: A F Maarten
authors.initials: AF
authors.lastname: Altelaar
authors.affiliation: Biomolecular Mass Spectrometry and Proteomics, Bijvoet Centre for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, University of Utrecht, Utrecht, The Netherlands.
authors.forename: Mirjam J
authors.initials: MJ
authors.lastname: Damen
authors.affiliation: Biophysics Program, Stanford University, Stanford, United States.
authors.forename: Kerwyn Casey
authors.initials: KC
authors.lastname: Huang
authors.affiliation: Institut de Biologie Structurale, Université Grenoble Alpes, Grenoble, France.
authors.forename: Jean-Pierre
authors.initials: JP
authors.lastname: Simorre
authors.affiliation: Membrane Biochemistry and Biophysics, Bijvoet Centre for Biomolecular Research, University of Utrecht, Utrecht, The Netherlands.
authors.forename: Eefjan
authors.initials: E
authors.lastname: Breukink
authors.affiliation: Bacterial Cell Biology, Swammerdam Institute for Life Sciences, Faculty of Science, University of Amsterdam, Amsterdam, The Netherlands.
authors.forename: Tanneke
authors.initials: T
authors.lastname: den Blaauwen
authors.affiliation: Genome Biology Unit, European Molecular Biology Laboratory Heidelberg, Heidelberg, Germany.
authors.forename: Athanasios
authors.initials: A
authors.lastname: Typas
authors.affiliation: Department of Microbiology and Immunology, University of California, San Francisco, San Francisco, United States.
authors.forename: Carol A
authors.initials: CA
authors.lastname: Gross
authors.affiliation: Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle Upon Tyne, United Kingdom.
authors.forename: Waldemar
authors.initials: W
authors.lastname: Vollmer
mesh_terms: D002455:Cell Division / Q000502:physiology*; D002462:Cell Membrane / Q000378:metabolism / Q000502:physiology*; D002733:Chlorophenols; D017931:DNA Primers / Q000235:genetics; D004926:Escherichia coli / Q000502:physiology*; D029968:Escherichia coli Proteins / Q000378:metabolism*; D005697:Galactosides; D055786:Gene Knockout Techniques; D007091:Image Processing, Computer-Assisted; D008565:Membrane Proteins / Q000378:metabolism*; D008856:Microscopy, Fluorescence; D046915:Penicillin-Binding Proteins / Q000378:metabolism; D010457:Peptidoglycan / Q000096:biosynthesis*; D046928:Peptidoglycan Glycosyltransferase / Q000378:metabolism; D010957:Plasmids / Q000235:genetics; D046929:Serine-Type D-Ala-D-Ala Carboxypeptidase / Q000378:metabolism
chemical_list: D002733:Chlorophenols; D017931:DNA Primers; D029968:Escherichia coli Proteins; D005697:Galactosides; D008565:Membrane Proteins; D046915:Penicillin-Binding Proteins; D010457:Peptidoglycan; C459860:YbgF protein, E coli; C074184:chlorophenol red galactopyranoside; D046928:Peptidoglycan Glycosyltransferase; C478681:penicillin-binding protein 1B, E coli; D046929:Serine-Type D-Ala-D-Ala Carboxypeptidase
keywords: E. coli; cell division; cell envelope; infectious disease; microbiology; outer membrane; peptidoglycan