The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in Escherichia coli
Author:
Peters Katharina1, Kannan Suresh2, Rao Vincenzo A.1, Biboy Jacob1, Vollmer Daniela1, Erickson Stephen W.3, Lewis Richard J.1, Young Kevin D.2, Vollmer Waldemar1
Affiliation:
1. Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, United Kingdom 2. Department of Microbiology and Immunology, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USA 3. Department of Biostatistics, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USA
Abstract
ABSTRACT
Peptidoglycan (PG) is an essential structural component of the bacterial cell wall and maintains the integrity and shape of the cell by forming a continuous layer around the cytoplasmic membrane. The thin PG layer of
Escherichia coli
resides in the periplasm, a unique compartment whose composition and pH can vary depending on the local environment of the cell. Hence, the growth of the PG layer must be sufficiently robust to allow cell growth and division under different conditions. We have analyzed the PG composition of 28 mutants lacking multiple PG enzymes (penicillin-binding proteins [PBPs]) after growth in acidic or near-neutral-pH media. Statistical analysis of the muropeptide profiles identified
dd
-carboxypeptidases (DD-CPases) that were more active in cells grown at acidic pH. In particular, the absence of the DD-CPase PBP6b caused a significant increase in the pentapeptide content of PG as well as morphological defects when the cells were grown at acidic pH. Other DD-CPases (PBP4, PBP4b, PBP5, PBP6a, PBP7, and AmpH) and the PG synthase PBP1B made a smaller or null contribution to the pentapeptide-trimming activity at acidic pH. We solved the crystal structure of PBP6b and also demonstrated that the enzyme is more stable and has a lower
K
m
at acidic pH, explaining why PBP6b is more active at low pH. Hence, PBP6b is a specialized DD-CPase that contributes to cell shape maintenance at low pH, and
E. coli
appears to utilize redundant DD-CPases for normal growth under different conditions.
IMPORTANCE
Escherichia coli
requires peptidoglycan
dd
-carboxypeptidases to maintain cell shape by controlling the amount of pentapeptide substrates available to the peptidoglycan synthetic transpeptidases. Why
E. coli
has eight, seemingly redundant
dd
-carboxypeptidases has remained unknown. We now show that one of these
dd
-carboxypeptidases, PBP6b, is important for cell shape maintenance in acidic growth medium, consistent with the higher activity and stability of the enzyme at low pH. Hence, the presence of multiple
dd
-carboxypeptidases with different enzymatic properties may allow
E. coli
to maintain a normal cell shape under various growth conditions.
Funder
Wellcome Trust Biotechnology and Biological Sciences Research Council HHS | NIH | NIH Office of the Director
Publisher
American Society for Microbiology
Subject
Virology,Microbiology
Reference62 articles.
1. Ingraham JL, Marr AG. 1996. Effect of temperature, pressure, pH, and osmotic stress on growth, p 1570–1578. In Neidhardt FC, Curtiss R, III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed), Escherichia coli and Salmonella: cellular and molecular biology, vol 2. ASM Press, Washington, DC. 2. Structural and functional properties of porin channels in E. coli outer membranes;Rosenbusch JP;Experientia,1990 3. Peptidoglycan structure and architecture 4. From the regulation of peptidoglycan synthesis to bacterial growth and morphology 5. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis
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