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 PBP1 B). 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.

DOI: http://dx.doi.org/10.7554/eLife.07118.001

eLife digest

All bacterial cells are surrounded by a membrane, which forms a protective barrier around the cell. Most bacteria also have a wall surrounding the membrane, which provides structural support. When a bacterial cell divides to produce two daughter cells, it produces a belt-like structure around the middle of the cell. This brings the membrane and cell wall on each side together to a ‘pinch-point’ until the two halves of the cell have been separated. This process must be carefully controlled to ensure that the cell does not burst open at any point.

Some bacteria known as ‘Gram-negative’ bacteria have a second membrane on the other side of the cell wall. These cells divide in the same way as other bacteria, but the need to coordinate the movement of three structures instead of two makes it more complicated. Many proteins are known to be involved. For example, one group (or ‘complex’) of proteins—which includes a protein called PBP1B—helps to produce new cell wall material. Another complex called the Tol system provides the energy needed for the outer membrane to be pulled inwards towards the pinch point. However, it has not been clear how these complexes work together to allow the cell to divide.

Here, Gray, Egan et al. searched for proteins that can interact with PBP1B during cell division in the Gram-negative bacterium E. coli. The experiments found that a protein called CpoB interacts with both PBP1B and the Tol system. CpoB is found in a band around the middle of the cell, and it regulates the activity of PBP1B in response to signals from the Tol system. If the activity of CpoB is disrupted, cell wall production and the movement of the outer membrane are no longer coordinated, and the membrane falls apart, leading to the death of the bacteria.

Gray, Egan et al.'s findings show how the production of new cell wall material can be linked to the inwards movement of the outer membrane during cell division. The next challenges are to understand the precise details of how these processes are coordinated by CpoB and to find out whether CpoB also plays the same role in other bacteria.

DOI: http://dx.doi.org/10.7554/eLife.07118.002