Wall teichoic acids regulate peptidoglycan synthesis by paving cell wall microstructure

Author:

Barber FelixORCID,Yuan Zhe,Akbary Zarina,Biboy Jacob,Vollmer Waldemar,Rojas Enrique R.

Abstract

AbstractThe Gram-positive cell wall is a rigid polysaccharide-peptide network that bears the cell’s turgor pressure and confers cell shape. In rod-shaped bacteria, the Rod complex inserts peptidoglycan polymers into the cell wall circumferentially, generating material anisotropy that promotes anisotropic growth. Wall teichoic acids, an abundant, non-load-bearing component of the Gram-positive cell wall, are also essential for rod-shape for unknown reasons. Here, we report a direct role for wall teichoic acids in anisotropic peptidoglycan synthesis. We show that wall teichoic acids provide a cohesive cell wall substrate that is required for Rod complex activity; conversely, removing wall teichoic acids yields a porous cell wall incapable of sustaining Rod complex activity. Consistent with this, cell elongation and Rod complex motion arrest in cells depleted for wall teichoic acids, but resume following hyperosmotic shocks that contract the cell wall. We further show that cells lacking wall teichoic acids rely instead on the bifunctional peptidoglycan synthesis enzyme PBP1, whose isotropic peptidoglycan synthesis is responsible for the subsequent growth and loss of shape. Taken together, these findings reveal that the microstructure of the Gram-positive cell wall is an essential regulatory factor in its own synthesis.SummaryThe bacterial cell wall is an essential macromolecule that encapsulates the cell and confers cell shape. Here, we reveal that an abundant yet understudied cell wall component in Gram-positive bacteria, wall teichoic acids, facilitates cell wall synthesis in the rod-shaped model organismBacillus subtilisby conferring a physically cohesive substrate for cell wall biosynthetic enzymes. This finding explains the decades-old mystery of why cells that lack wall teichoic acids lose cell shape and grow slowly, while also highlighting an underappreciated factor impacting cell wall homeostasis: the microstructure of the wall itself.

Publisher

Cold Spring Harbor Laboratory

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