FtsZ Collaborates with Penicillin Binding Proteins To Generate Bacterial Cell Shape inEscherichia coli

Abstract

The mechanisms by which bacteria adopt and maintain individual shapes remain enigmatic. Outstanding questions include why cells are a certain size, length, and width; why they are uniform or irregular; and why some branch while others do not. Previously, we showed that Escherichia coli mutants lacking multiple penicillin binding proteins (PBPs) display extensive morphological diversity. Because defective sites in these cells exhibit the structural and functional characteristics of improperly localized poles, we investigated the connection between cell division and shape. Here we show that under semipermissive conditions the temperature-sensitive FtsZ84 protein produces branched and aberrant cells at a high frequency in mutants lacking PBP 5, and this phenotype is exacerbated by the loss of additional peptidoglycan endopeptidases. Surprisingly, certain ftsZ84 strains lyse at the nonpermissive temperature instead of filamenting, and inhibition of wild-type FtsZ forces some mutants into tightly wound spirillum-like morphologies. The results demonstrate that significant aspects of bacterial shape are dictated by a previously unrecognized relationship between the septation machinery and ostensibly minor peptidoglycan-modifying enzymes and that under certain circumstances improper FtsZ function can destroy the structural integrity of the cell.

Crystal Structure of the Actinomadura R39 DD-peptidase Reveals New Domains in Penicillin-binding Proteins

“…The resemblance of the R39 domain II topology with E. coli d-Tyr-tRNA Tyr deacylase and barley 1,3-1,4-␤-glucanase is astonishing but seems unlikely to be associated with the functional properties of these enzymes. Although B. subtilis PBP4a was shown to be absent from the septum site (49), it is interesting that interactions between proteins of the septation machinery and minor peptidoglycan-modifying enzymes have been shown to be responsible for significant aspects of bacterial shape determinations (50). Although very limited, the resemblance of R39 domain II to the N-terminal domain of MinC and the 1A region of FtsA, two proteins involved in the regulation of septum formation, suggests that class C low molecular mass PBPs could interact with a protein of the septation machinery.…”

How Bacteria Consume Their Own Exoskeletons (Turnover and Recycling of Cell Wall Peptidoglycan)

“…Mutations in some of the PG hydrolases affect septum cleavage (45) and also cell shape (78,98,100,125,133).…”

Bacterial Cell Wall Synthesis: New Insights from Localization Studies

“…Another indication linking FtsZ to cell shape determination was the observation that the formation of branches and abnormal cell shapes observed in mutants lacking LMW PBPs, notably PBP5 (42,134), was augmented when these mutants were studied in an ftsZ84(Ts) background (193). Mutant cells lacking PBP5 and another LMW PBP (the phenomenon was strictly PBP5 dependent) showed spiral morphology when FtsZ activity was blocked by overexpression of the FtsZ inhibitor SulA (193).…”

“…Mutant cells lacking PBP5 and another LMW PBP (the phenomenon was strictly PBP5 dependent) showed spiral morphology when FtsZ activity was blocked by overexpression of the FtsZ inhibitor SulA (193). PBP5 is the major carboxypeptidase but is not specifically associated with cell division.…”