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Crit Rev Microbiol. 1998;24(1):23-59.

The biophysics of the gram-negative periplasmic space.

Author information

1
Biology Department, Indiana University, Bloomington 47405-6801, USA.

Abstract

When subject to an osmotic 'up-shock', water flows outward from bacterial cytoplasm of the bacterium. Lipid bilayers can shrink very little in area and therefore must wrinkle to accommodate the smaller volume. The usual consequence is that all the layers of the cell envelope must become wrinkled together because they adhere to each other and must now cover a smaller surface. Plasmolysis spaces are formed if the cytoplasmic membrane (CM) separates from the other components of the wall. However, because the CM bilayer is essentially an incompressible two-dimensional liquid, this constraint restricts the location and shape of plasmolysis spaces. With mild up-shocks they form at the pole and around constricting regions in the cell. Elsewhere their creation requires the formation of endocytotic or exocytotic vesicles. The formation of endocytotic vesicles occurs in animal and plant cells as well as in bacterial cells. With stronger up-shocks tubular structures (Bayer adhesion sites), or other special geometric shapes (e.g., Scheie structures) allow the bilayer to surround an irregular shaped cytoplast. Periosmotic agents, that is, those that extract water from the periplasm as well as the cytoplasm, are molecules such as poly-vinyl-pyrrolidone and alpha-cyclodextrin that are too large to pass through the porins in the outer membrane. They were found to significantly inhibit the formation of plasmolysis spaces. Presumably, they inhibit the plasmolysis process, which requires that extracellular fluid enter between the CM and the outer membrane (OM). In the extreme case, with the dehydrating action of both osmotic agents and periosmotic agents, periplasmic space formation tends to be prevented and a new kind of space develops within the cytoplasm. We have designated these as 'cytoplasmic voids'. These novel structures are not bounded by lipid bilayers, in contrast to the endocytotic vesicles. These new spaces appear to result from the negative turgor pressure generated by the application of the combination of osmotic and periosmotic agents causing bubble formation. Several ideas in the literature about the wall biology (periseptal annuli, leading edge, osmotic pressure in the periplasm) are presented and critiqued. The basic criticism of these is that much of the phenomena can be explained because of the physics of the phospholipid bilayers and osmotic forces and thus does not imply the existence of a special control mechanism to regulate growth and division.

PMID:
9561823
DOI:
10.1080/10408419891294172
[Indexed for MEDLINE]

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