The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in <named-content content-type="genus-species">Escherichia coli</named-content>

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 comp...

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Autores principales:	Katharina Peters, Suresh Kannan, Vincenzo A. Rao, Jacob Biboy, Daniela Vollmer, Stephen W. Erickson, Richard J. Lewis, Kevin D. Young, Waldemar Vollmer
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/052dc59cc17e4054b7b6eb40eedfde7e
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spelling	oai:doaj.org-article:052dc59cc17e4054b7b6eb40eedfde7e2021-11-15T15:50:16ZThe Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in <named-content content-type="genus-species">Escherichia coli</named-content>10.1128/mBio.00819-162150-7511https://doaj.org/article/052dc59cc17e4054b7b6eb40eedfde7e2016-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00819-16https://doaj.org/toc/2150-7511ABSTRACT 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 Km 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.Katharina PetersSuresh KannanVincenzo A. RaoJacob BiboyDaniela VollmerStephen W. EricksonRichard J. LewisKevin D. YoungWaldemar VollmerAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 3 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Katharina Peters Suresh Kannan Vincenzo A. Rao Jacob Biboy Daniela Vollmer Stephen W. Erickson Richard J. Lewis Kevin D. Young Waldemar Vollmer The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in <named-content content-type="genus-species">Escherichia coli</named-content>
description	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 Km 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.
format	article
author	Katharina Peters Suresh Kannan Vincenzo A. Rao Jacob Biboy Daniela Vollmer Stephen W. Erickson Richard J. Lewis Kevin D. Young Waldemar Vollmer
author_facet	Katharina Peters Suresh Kannan Vincenzo A. Rao Jacob Biboy Daniela Vollmer Stephen W. Erickson Richard J. Lewis Kevin D. Young Waldemar Vollmer
author_sort	Katharina Peters
title	The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in <named-content content-type="genus-species">Escherichia coli</named-content>
title_short	The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full	The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in <named-content content-type="genus-species">Escherichia coli</named-content>
title_fullStr	The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full_unstemmed	The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in <named-content content-type="genus-species">Escherichia coli</named-content>
title_sort	redundancy of peptidoglycan carboxypeptidases ensures robust cell shape maintenance in <named-content content-type="genus-species">escherichia coli</named-content>
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/052dc59cc17e4054b7b6eb40eedfde7e
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The Redundancy of Peptidoglycan Carboxypeptidases Ensures Robust Cell Shape Maintenance in <named-content content-type="genus-species">Escherichia coli</named-content>

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