How Teichoic Acids Could Support a Periplasm in Gram-Positive Bacteria, and Let Cell Division Cheat Turgor Pressure

Abstract

The cytoplasm of bacteria is maintained at a higher osmolality than the growth medium, which generates a turgor pressure. The cell membrane (CM) cannot support a large turgor, so there are two possibilities for transferring the pressure to the peptidoglycan cell wall (PGW): (1) the CM could be pressed directly against the PGW, or (2) the CM could be separated from the PGW by a periplasmic space that is isoosmotic with the cytoplasm. There is strong evidence for gram-negative bacteria that a periplasm exists and is isoosmotic with the cytoplasm. No comparable studies have been done for gram-positive bacteria. Here I suggest that a periplasmic space is probably essential in order for the periplasmic proteins to function, including especially the PBPs that remodel the peptidoglycan wall. I then present a semi-quantitative analysis of how teichoic acids could support a periplasm that is isoosmotic with the cytoplasm. The fixed anionic charge density of teichoic acids in the periplasm is ∼0.5 M, which would bring in ∼0.5 M Na+ neutralizing ions. This approximately balances the excess osmolality of the cytoplasm that would produce a turgor pressure of 19 atm. The 0.5 M fixed charge density is similar to that of proteoglycans in articular cartilage, suggesting a comparability ability to support pressure. An isoosmotic periplasm would be especially important for cell division, since it would allow CM constriction and PGW synthesis to avoid turgor pressure.

Understanding Beta-Lactam-Induced Lysis at the Single-Cell Level

“…This assumption is consistent with viewing the periplasm as an effectively rigid body. We have previously suggested (Hussain et al, 2018 ) that a case in which the cytoplasm is isoosmotic with the periplasm (Sochacki et al, 2011 ; Erickson, 2017 , 2021 ), such that the OM is effectively rigid and the only load-bearing layer of the cellular envelope, is inconsistent with the mechanical stability of the periplasm because the bending energies of the membranes in Equation (1) are smaller for cylindrical shapes of larger radius: thus, in rod-like cells with sufficient IM surface area, the IM is predicted to press against the cell wall and OM and squeeze out any isoosmotic periplasmic space (see Hussain et al, 2018 for a detailed discussion). Nevertheless, this case can be accommodated in our model by (1) setting K = 0 and the elastic moduli of the cell wall, Y w , to be that of the rigid OM in the cylindrical bulk of the cell, and (2) viewing K as the area-stretch modulus of the cell wall-decoupled, fluid OM in the bulge.…”

The Staphylococcus aureus cell division protein, DivIC, interacts with the cell wall and controls its biosynthesis

“…Covalently bound to the PG are WTA that alters the charge and has a number of cellular functions 43 . Collectively the teichoic acids are essential for cell viability 43 and have been proposed to be responsible for the maintenance of the exoplasm (the region between the cytoplasmic membrane and PG 54 ), in which the final stages of PG biosynthesis takes place 55 . Not only are there PG architectural changes during division but also teichoic acid dynamics.…”

Remodeling of the Enterococcal Cell Envelope during Surface Penetration Promotes Intrinsic Resistance to Stress

“…Gram-positive bacteria possess a tripartite cell wall ( 24 , 75 , 76 ), in which the inner electron-dark area (such as CE-1; Fig. 1D ), localized between the outer face of the membrane and the peptidoglycan layer (intermediate electron-translucent region), is considered the periplasm ( 24 , 75 – 77 ). In Bacillus subtilis , this periplasmic space was shown to be formed by membrane-linked lipoteichoic acids, or LTAs ( 77 ).…”