Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division

Andrew N Gray; Alexander J F Egan; Inge van 't Veer; Jolanda Verheul; Alexandre Colavin; Alexandra Koumoutsi; Jacob Biboy; A F Maarten Altelaar; Mirjam J Damen; Kerwyn Casey Huang; Jean-Pierre Simorre; Eefjan Breukink; Tanneke den Blaauwen; Athanasios Typas; Carol A Gross; Waldemar Vollmer

doi:10.7554/eLife.07118

Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division

Andrew N Gray, Alexander J F Egan, Inge van 't Veer, Jolanda Verheul, Alexandre Colavin, Alexandra Koumoutsi, Jacob Biboy, A F Maarten Altelaar, Mirjam J Damen, Kerwyn Casey Huang, Jean-Pierre Simorre, Eefjan Breukink, Tanneke den Blaauwen, Athanasios Typas, Carol A Gross, Waldemar Vollmer

Research output: Contribution to journal › Article › Academic › peer-review

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.

Original language	English
Journal	eLife
Volume	4
DOIs	https://doi.org/10.7554/eLife.07118
Publication status	Published - 7 May 2015

Keywords

PENICILLIN-BINDING PROTEINS
BETA-LACTAM ANTIBIOTICS
N-TERMINAL DOMAIN
MUREIN-LIPOPROTEIN
BACILLUS-SUBTILIS
CYTOKINETIC RING
WALL HYDROLYSIS
INNER MEMBRANE
SYNTHASE PBP1B
INDUCED LYSIS

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Gray, A. N., Egan, A. J. F., van 't Veer, I., Verheul, J., Colavin, A., Koumoutsi, A., Biboy, J., Altelaar, A. F. M., Damen, M. J., Huang, K. C., Simorre, J.-P., Breukink, E., den Blaauwen, T., Typas, A., Gross, C. A., & Vollmer, W. (2015). Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division. eLife, 4. https://doi.org/10.7554/eLife.07118

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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.",

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AU - Egan, Alexander J F

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AU - Colavin, Alexandre

AU - Koumoutsi, Alexandra

AU - Biboy, Jacob

AU - Altelaar, A F Maarten

AU - Damen, Mirjam J

AU - Huang, Kerwyn Casey

AU - Simorre, Jean-Pierre

AU - Breukink, Eefjan

AU - den Blaauwen, Tanneke

AU - Typas, Athanasios

AU - Gross, Carol A

AU - Vollmer, Waldemar

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N2 - 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.

AB - 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.

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KW - N-TERMINAL DOMAIN

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KW - CYTOKINETIC RING

KW - WALL HYDROLYSIS

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KW - INDUCED LYSIS

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JO - eLife

JF - eLife

ER -

Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division

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