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...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2020-12-01
|
| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02796-20 |
| _version_ | 1818751053577846784 |
|---|---|
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-18T04:29:27Z |
| format | Article |
| id | doaj.art-77e5c353684b43e199be94315c973b14 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-18T04:29:27Z |
| publishDate | 2020-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-77e5c353684b43e199be94315c973b142022-12-21T21:21:01ZengAmerican Society for MicrobiologymBio2150-75112020-12-0111610.1128/mBio.02796-20SPOR Proteins Are Required for Functionality of Class A Penicillin-Binding Proteins in <named-content content-type="genus-species">Escherichia coli</named-content>Manuel Pazos0Katharina Peters1Adrien Boes2Yalda Safaei3Calem Kenward4Nathanael A. Caveney5Cedric Laguri6Eefjan Breukink7Natalie C. J. Strynadka8Jean-Pierre Simorre9Mohammed Terrak10Waldemar Vollmer11Centre for Bacterial Cell Biology, Biosciences Institute, Newcastle University, Newcastle upon Tyne, United KingdomCentre for Bacterial Cell Biology, Biosciences Institute, Newcastle University, Newcastle upon Tyne, United KingdomInBioS–Centre d'Ingénierie des Protéines, Liège University, Liège, BelgiumBiochemistry and Molecular Biology and Centre for Blood Research, The University of British Columbia, Vancouver, British Columbia, CanadaBiochemistry and Molecular Biology and Centre for Blood Research, The University of British Columbia, Vancouver, British Columbia, CanadaDepartment of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, California, USAUniversity of Grenoble Alpes, CNRS, CEA, IBS, Grenoble, FranceMembrane Biochemistry and Biophysics, Department of Chemistry, Faculty of Science, Utrecht University, Utrecht, The NetherlandsBiochemistry and Molecular Biology and Centre for Blood Research, The University of British Columbia, Vancouver, British Columbia, CanadaUniversity of Grenoble Alpes, CNRS, CEA, IBS, Grenoble, FranceInBioS–Centre d'Ingénierie des Protéines, Liège University, Liège, BelgiumCentre for Bacterial Cell Biology, Biosciences Institute, Newcastle University, Newcastle upon Tyne, United KingdomABSTRACT 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.https://journals.asm.org/doi/10.1128/mBio.02796-20SPOR domaincell divisionpeptidoglycanpeptidoglycan synthases |
| spellingShingle | 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> mBio SPOR domain cell division peptidoglycan peptidoglycan synthases |
| 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_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_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_sort | spor proteins are required for functionality of class a penicillin binding proteins in named content content type genus species escherichia coli named content |
| topic | SPOR domain cell division peptidoglycan peptidoglycan synthases |
| url | https://journals.asm.org/doi/10.1128/mBio.02796-20 |
| work_keys_str_mv | AT manuelpazos sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT katharinapeters sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT adrienboes sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT yaldasafaei sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT calemkenward sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT nathanaelacaveney sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT cedriclaguri sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT eefjanbreukink sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT nataliecjstrynadka sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT jeanpierresimorre sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT mohammedterrak sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent AT waldemarvollmer sporproteinsarerequiredforfunctionalityofclassapenicillinbindingproteinsinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontent |