SPOR Proteins Are Required for Functionality of Class A Penicillin-Binding Proteins in <named-content content-type="genus-species">Escherichia coli</named-content>

ABSTRACT Sporulation-related repeat (SPOR) domains are present in many bacterial cell envelope proteins and are known to bind peptidoglycan. Escherichia coli contains four SPOR proteins, DamX, DedD, FtsN, and RlpA, of which FtsN is essential for septal peptidoglycan synthesis. DamX and DedD may also...

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Autores principales:	Manuel Pazos, Katharina Peters, Adrien Boes, Yalda Safaei, Calem Kenward, Nathanael A. Caveney, Cedric Laguri, Eefjan Breukink, Natalie C. J. Strynadka, Jean-Pierre Simorre, Mohammed Terrak, Waldemar Vollmer
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	SPOR domain cell division peptidoglycan peptidoglycan synthases Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/77e5c353684b43e199be94315c973b14
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spelling	oai:doaj.org-article:77e5c353684b43e199be94315c973b142021-11-15T15:55:43ZSPOR Proteins Are Required for Functionality of Class A Penicillin-Binding Proteins in <named-content content-type="genus-species">Escherichia coli</named-content>10.1128/mBio.02796-202150-7511https://doaj.org/article/77e5c353684b43e199be94315c973b142020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02796-20https://doaj.org/toc/2150-7511ABSTRACT Sporulation-related repeat (SPOR) domains are present in many bacterial cell envelope proteins and are known to bind peptidoglycan. Escherichia coli contains four SPOR proteins, DamX, DedD, FtsN, and RlpA, of which FtsN is essential for septal peptidoglycan synthesis. DamX and DedD may also play a role in cell division, based on mild cell division defects observed in strains lacking these SPOR domain proteins. Here, we show by nuclear magnetic resonance (NMR) spectroscopy that the periplasmic part of DedD consists of a disordered region followed by a canonical SPOR domain with a structure similar to that of the SPOR domains of FtsN, DamX, and RlpA. The absence of DamX or DedD decreases the functionality of the bifunctional transglycosylase-transpeptidase penicillin-binding protein 1B (PBP1B). DamX and DedD interact with PBP1B and stimulate its glycosyltransferase activity, and DamX also stimulates the transpeptidase activity. DedD also binds to PBP1A and stimulates its glycosyltransferase activity. Our data support a direct role of DamX and DedD in enhancing the activity of PBP1B and PBP1A, presumably during the synthesis of the cell division septum. IMPORTANCE Escherichia coli has four SPOR proteins that bind peptidoglycan, of which FtsN is essential for cell division. DamX and DedD are suggested to have semiredundant functions in cell division based on genetic evidence. Here, we solved the structure of the SPOR domain of DedD, and we show that both DamX and DedD interact with and stimulate the synthetic activity of the peptidoglycan synthases PBP1A and PBP1B, suggesting that these class A PBP enzymes act in concert with peptidoglycan-binding proteins during cell division.Manuel PazosKatharina PetersAdrien BoesYalda SafaeiCalem KenwardNathanael A. CaveneyCedric LaguriEefjan BreukinkNatalie C. J. StrynadkaJean-Pierre SimorreMohammed TerrakWaldemar VollmerAmerican Society for MicrobiologyarticleSPOR domaincell divisionpeptidoglycanpeptidoglycan synthasesMicrobiologyQR1-502ENmBio, Vol 11, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	SPOR domain cell division peptidoglycan peptidoglycan synthases Microbiology QR1-502
spellingShingle	SPOR domain cell division peptidoglycan peptidoglycan synthases Microbiology QR1-502 Manuel Pazos Katharina Peters Adrien Boes Yalda Safaei Calem Kenward Nathanael A. Caveney Cedric Laguri Eefjan Breukink Natalie C. J. Strynadka Jean-Pierre Simorre Mohammed Terrak Waldemar Vollmer SPOR Proteins Are Required for Functionality of Class A Penicillin-Binding Proteins in <named-content content-type="genus-species">Escherichia coli</named-content>
description	ABSTRACT Sporulation-related repeat (SPOR) domains are present in many bacterial cell envelope proteins and are known to bind peptidoglycan. Escherichia coli contains four SPOR proteins, DamX, DedD, FtsN, and RlpA, of which FtsN is essential for septal peptidoglycan synthesis. DamX and DedD may also play a role in cell division, based on mild cell division defects observed in strains lacking these SPOR domain proteins. Here, we show by nuclear magnetic resonance (NMR) spectroscopy that the periplasmic part of DedD consists of a disordered region followed by a canonical SPOR domain with a structure similar to that of the SPOR domains of FtsN, DamX, and RlpA. The absence of DamX or DedD decreases the functionality of the bifunctional transglycosylase-transpeptidase penicillin-binding protein 1B (PBP1B). DamX and DedD interact with PBP1B and stimulate its glycosyltransferase activity, and DamX also stimulates the transpeptidase activity. DedD also binds to PBP1A and stimulates its glycosyltransferase activity. Our data support a direct role of DamX and DedD in enhancing the activity of PBP1B and PBP1A, presumably during the synthesis of the cell division septum. IMPORTANCE Escherichia coli has four SPOR proteins that bind peptidoglycan, of which FtsN is essential for cell division. DamX and DedD are suggested to have semiredundant functions in cell division based on genetic evidence. Here, we solved the structure of the SPOR domain of DedD, and we show that both DamX and DedD interact with and stimulate the synthetic activity of the peptidoglycan synthases PBP1A and PBP1B, suggesting that these class A PBP enzymes act in concert with peptidoglycan-binding proteins during cell division.
format	article
author	Manuel Pazos Katharina Peters Adrien Boes Yalda Safaei Calem Kenward Nathanael A. Caveney Cedric Laguri Eefjan Breukink Natalie C. J. Strynadka Jean-Pierre Simorre Mohammed Terrak Waldemar Vollmer
author_facet	Manuel Pazos Katharina Peters Adrien Boes Yalda Safaei Calem Kenward Nathanael A. Caveney Cedric Laguri Eefjan Breukink Natalie C. J. Strynadka Jean-Pierre Simorre Mohammed Terrak Waldemar Vollmer
author_sort	Manuel Pazos
title	SPOR Proteins Are Required for Functionality of Class A Penicillin-Binding Proteins in <named-content content-type="genus-species">Escherichia coli</named-content>
title_short	SPOR Proteins Are Required for Functionality of Class A Penicillin-Binding Proteins in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full	SPOR Proteins Are Required for Functionality of Class A Penicillin-Binding Proteins in <named-content content-type="genus-species">Escherichia coli</named-content>
title_fullStr	SPOR Proteins Are Required for Functionality of Class A Penicillin-Binding Proteins in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full_unstemmed	SPOR Proteins Are Required for Functionality of Class A Penicillin-Binding Proteins in <named-content content-type="genus-species">Escherichia coli</named-content>
title_sort	spor proteins are required for functionality of class a penicillin-binding proteins in <named-content content-type="genus-species">escherichia coli</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/77e5c353684b43e199be94315c973b14
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SPOR Proteins Are Required for Functionality of Class A Penicillin-Binding Proteins in <named-content content-type="genus-species">Escherichia coli</named-content>

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