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The outer membrane lipoprotein NlpI nucleates hydrolases within peptidoglycan multi-enzyme complexes in Escherichia coli

Manuel Banzhaf, Hamish C. L. Yau, Jolanda Verheul, Adam Lodge, George Kritikos, André Mateus, Ann Kristin Hov, Frank Stein, Morgane Wartel, Manuel Pazos, Alexandra S. Solovyova, Mikhail M Savitski, Tanneke den Blaauwen, Athanasios Typas, Waldemar Vollmer
doi: https://doi.org/10.1101/609503
Manuel Banzhaf
1European Molecular Biology Laboratory, Genome Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
2Institute of Microbiology & Infection and School of Biosciences, University of Birmingham, Edgbaston, Birmingham, UK. B15 2TT
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Hamish C. L. Yau
3Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, NE2 4AX, Newcastle upon Tyne, United Kingdom
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Jolanda Verheul
4Bacterial Cell Biology & Physiology, Swammerdam Institute for Life Sciences, Faculty of Science, University of Amsterdam; Science Park 904, 1098 XH Amsterdam, The Netherlands
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Adam Lodge
3Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, NE2 4AX, Newcastle upon Tyne, United Kingdom
7Iksuda therapeutics, The Biosphere, Newcastle upon Tyne, NE4 5BX
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George Kritikos
1European Molecular Biology Laboratory, Genome Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
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André Mateus
1European Molecular Biology Laboratory, Genome Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
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Ann Kristin Hov
1European Molecular Biology Laboratory, Genome Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
8École polytechnique fédérale de Lausanne SV IBI-SV UPDALPE AAB 013, station 19, 1015 Lausanne, Switzerland
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Frank Stein
1European Molecular Biology Laboratory, Genome Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
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Morgane Wartel
1European Molecular Biology Laboratory, Genome Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
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Manuel Pazos
3Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, NE2 4AX, Newcastle upon Tyne, United Kingdom
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Alexandra S. Solovyova
5Newcastle University Protein and Proteome Analysis, Devonshire Building, Devonshire Terrace, Newcastle upon Tyne, NE1 7RU, UK
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Mikhail M Savitski
1European Molecular Biology Laboratory, Genome Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
6European Molecular Biology Laboratory, Structural & Computational Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
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Tanneke den Blaauwen
4Bacterial Cell Biology & Physiology, Swammerdam Institute for Life Sciences, Faculty of Science, University of Amsterdam; Science Park 904, 1098 XH Amsterdam, The Netherlands
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  • For correspondence: T.denBlaauwen@uva.nl typas@embl.de w.vollmer@ncl.ac.uk
Athanasios Typas
1European Molecular Biology Laboratory, Genome Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
6European Molecular Biology Laboratory, Structural & Computational Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
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  • For correspondence: T.denBlaauwen@uva.nl typas@embl.de w.vollmer@ncl.ac.uk
Waldemar Vollmer
3Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, NE2 4AX, Newcastle upon Tyne, United Kingdom
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  • For correspondence: T.denBlaauwen@uva.nl typas@embl.de w.vollmer@ncl.ac.uk
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Abstract

The peptidoglycan (PG) sacculus provides bacteria with the mechanical strength to maintain cell shape and resist osmotic stress. Enlargement of the mesh-like sacculus requires the combined activity of PG synthases and hydrolases. In Escherichia coli, the activity of the two bifunctional PG synthases is driven by lipoproteins anchored in the outer membrane. However, the regulation of PG hydrolases is less well understood, with only regulators for PG amidases having been described. Here, we identify the lipoprotein NlpI as a general adaptor protein for PG hydrolases. NlpI binds to different classes of hydrolases and can specifically form multimeric complexes with various PG endopeptidases. In addition, NlpI seems to contribute both to PG elongation and cell division biosynthetic complexes based on its localization and genetic interactions. In line with such a role, we reconstitute PG multi-enzyme complexes containing NlpI, the PG synthesis regulator LpoA, its cognate bifunctional synthase, PBP1A, and different endopeptidases. Our results indicate that PG regulators and adaptors are part of PG biosynthetic multi-enzyme complexes, regulating and potentially coordinating the spatiotemporal action of PG synthases and hydrolases.

Significance The activity of PG hydrolases may cause lysis of the bacterial cell if left unregulated. Hence, the cell must have ways of regulating and coordinating their activities. Our current understanding of how this occurs is incomplete. In this work, we present the outer membrane (OM) anchored lipoprotein, NlpI, as a scaffold of peptidoglycan hydrolases. We propose that NlpI facilitates the formation of multi-enzyme complexes and that, along with other regulators, it coordinates a safe enlargement and separation of the PG layer in E. coli.

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Posted April 16, 2019.
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The outer membrane lipoprotein NlpI nucleates hydrolases within peptidoglycan multi-enzyme complexes in Escherichia coli
Manuel Banzhaf, Hamish C. L. Yau, Jolanda Verheul, Adam Lodge, George Kritikos, André Mateus, Ann Kristin Hov, Frank Stein, Morgane Wartel, Manuel Pazos, Alexandra S. Solovyova, Mikhail M Savitski, Tanneke den Blaauwen, Athanasios Typas, Waldemar Vollmer
bioRxiv 609503; doi: https://doi.org/10.1101/609503
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The outer membrane lipoprotein NlpI nucleates hydrolases within peptidoglycan multi-enzyme complexes in Escherichia coli
Manuel Banzhaf, Hamish C. L. Yau, Jolanda Verheul, Adam Lodge, George Kritikos, André Mateus, Ann Kristin Hov, Frank Stein, Morgane Wartel, Manuel Pazos, Alexandra S. Solovyova, Mikhail M Savitski, Tanneke den Blaauwen, Athanasios Typas, Waldemar Vollmer
bioRxiv 609503; doi: https://doi.org/10.1101/609503

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