The Pseudomonas aeruginosa T6SS Delivers a Periplasmic Toxin that Disrupts Bacterial Cell Morphology

The type VI secretion system (T6SS) is crucial in interbacterial competition and is a virulence determinant of many Gram-negative bacteria. Several T6SS effectors are covalently fused to secreted T6SS structural components such as the VgrG spike for delivery into target cells. In Pseudomonas aerugin...

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Published inCell reports (Cambridge) Vol. 29; no. 1; pp. 187 - 201.e7
Main Authors Wood, Thomas E., Howard, Sophie A., Förster, Andreas, Nolan, Laura M., Manoli, Eleni, Bullen, Nathan P., Yau, Hamish C.L., Hachani, Abderrahman, Hayward, Richard D., Whitney, John C., Vollmer, Waldemar, Freemont, Paul S., Filloux, Alain
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.10.2019
Cell Press
Elsevier
Subjects
Anti-Bacterial Agents - pharmacology
Bacterial Proteins - metabolism
Bacterial Secretion Systems - metabolism
Bacterial Secretion Systems - physiology
beta-Lactams - metabolism
effector
metallopeptidase
Periplasm - drug effects
Periplasm - metabolism
Periplasm - physiology
Pseudomonas aeruginosa
Pseudomonas aeruginosa - drug effects
Pseudomonas aeruginosa - metabolism
Pseudomonas aeruginosa - physiology
type VI secretion system
Type VI Secretion Systems - metabolism
Type VI Secretion Systems - physiology
VgrG
Virulence Factors - metabolism
Pseudomonas aeruginosa
effector
type VI secretion system
metallopeptidase
VgrG
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Abstract The type VI secretion system (T6SS) is crucial in interbacterial competition and is a virulence determinant of many Gram-negative bacteria. Several T6SS effectors are covalently fused to secreted T6SS structural components such as the VgrG spike for delivery into target cells. In Pseudomonas aeruginosa, the VgrG2b effector was previously proposed to mediate bacterial internalization into eukaryotic cells. In this work, we find that the VgrG2b C-terminal domain (VgrG2bC-ter) elicits toxicity in the bacterial periplasm, counteracted by a cognate immunity protein. We resolve the structure of VgrG2bC-ter and confirm it is a member of the zinc-metallopeptidase family of enzymes. We show that this effector causes membrane blebbing at midcell, which suggests a distinct type of T6SS-mediated growth inhibition through interference with cell division, mimicking the impact of β-lactam antibiotics. Our study introduces a further effector family to the T6SS arsenal and demonstrates that VgrG2b can target both prokaryotic and eukaryotic cells. [Display omitted] •The structure of the VgrG2b C-terminal domain presents a metallopeptidase fold•VgrG2b exerts antibacterial activity in the periplasmic space•Toxicity of VgrG2b is counteracted by a cognate periplasmic immunity protein•VgrG2bC-ter-intoxicated prey cells bleb at the midcell and lyse The bacterial type VI secretion system (T6SS) delivers effector proteins into prokaryotic and eukaryotic cells to enhance the survival of the donor cell. Wood et al. describe an antibacterial T6SS toxin family eliciting a profound cell division defect and lysis. The structure of this periplasmic-acting toxin reveals a metallopeptidase fold.
AbstractList The type VI secretion system (T6SS) is crucial in interbacterial competition and is a virulence determinant of many Gram-negative bacteria. Several T6SS effectors are covalently fused to secreted T6SS structural components such as the VgrG spike for delivery into target cells. In Pseudomonas aeruginosa , the VgrG2b effector was previously proposed to mediate bacterial internalization into eukaryotic cells. In this work, we find that the VgrG2b C-terminal domain (VgrG2b C-ter ) elicits toxicity in the bacterial periplasm, counteracted by a cognate immunity protein. We resolve the structure of VgrG2b C-ter and confirm it is a member of the zinc-metallopeptidase family of enzymes. We show that this effector causes membrane blebbing at midcell, which suggests a distinct type of T6SS-mediated growth inhibition through interference with cell division, mimicking the impact of β-lactam antibiotics. Our study introduces a further effector family to the T6SS arsenal and demonstrates that VgrG2b can target both prokaryotic and eukaryotic cells. • The structure of the VgrG2b C-terminal domain presents a metallopeptidase fold • VgrG2b exerts antibacterial activity in the periplasmic space • Toxicity of VgrG2b is counteracted by a cognate periplasmic immunity protein • VgrG2b C-ter -intoxicated prey cells bleb at the midcell and lyse The bacterial type VI secretion system (T6SS) delivers effector proteins into prokaryotic and eukaryotic cells to enhance the survival of the donor cell. Wood et al. describe an antibacterial T6SS toxin family eliciting a profound cell division defect and lysis. The structure of this periplasmic-acting toxin reveals a metallopeptidase fold.
The type VI secretion system (T6SS) is crucial in interbacterial competition and is a virulence determinant of many Gram-negative bacteria. Several T6SS effectors are covalently fused to secreted T6SS structural components such as the VgrG spike for delivery into target cells. In Pseudomonas aeruginosa, the VgrG2b effector was previously proposed to mediate bacterial internalization into eukaryotic cells. In this work, we find that the VgrG2b C-terminal domain (VgrG2b ) elicits toxicity in the bacterial periplasm, counteracted by a cognate immunity protein. We resolve the structure of VgrG2b and confirm it is a member of the zinc-metallopeptidase family of enzymes. We show that this effector causes membrane blebbing at midcell, which suggests a distinct type of T6SS-mediated growth inhibition through interference with cell division, mimicking the impact of β-lactam antibiotics. Our study introduces a further effector family to the T6SS arsenal and demonstrates that VgrG2b can target both prokaryotic and eukaryotic cells.
The type VI secretion system (T6SS) is crucial in interbacterial competition and is a virulence determinant of many Gram-negative bacteria. Several T6SS effectors are covalently fused to secreted T6SS structural components such as the VgrG spike for delivery into target cells. In Pseudomonas aeruginosa, the VgrG2b effector was previously proposed to mediate bacterial internalization into eukaryotic cells. In this work, we find that the VgrG2b C-terminal domain (VgrG2bC-ter) elicits toxicity in the bacterial periplasm, counteracted by a cognate immunity protein. We resolve the structure of VgrG2bC-ter and confirm it is a member of the zinc-metallopeptidase family of enzymes. We show that this effector causes membrane blebbing at midcell, which suggests a distinct type of T6SS-mediated growth inhibition through interference with cell division, mimicking the impact of β-lactam antibiotics. Our study introduces a further effector family to the T6SS arsenal and demonstrates that VgrG2b can target both prokaryotic and eukaryotic cells. : The bacterial type VI secretion system (T6SS) delivers effector proteins into prokaryotic and eukaryotic cells to enhance the survival of the donor cell. Wood et al. describe an antibacterial T6SS toxin family eliciting a profound cell division defect and lysis. The structure of this periplasmic-acting toxin reveals a metallopeptidase fold. Keywords: type VI secretion system, VgrG, effector, metallopeptidase, Pseudomonas aeruginosa
The type VI secretion system (T6SS) is crucial in interbacterial competition and is a virulence determinant of many Gram-negative bacteria. Several T6SS effectors are covalently fused to secreted T6SS structural components such as the VgrG spike for delivery into target cells. In Pseudomonas aeruginosa, the VgrG2b effector was previously proposed to mediate bacterial internalization into eukaryotic cells. In this work, we find that the VgrG2b C-terminal domain (VgrG2bC-ter) elicits toxicity in the bacterial periplasm, counteracted by a cognate immunity protein. We resolve the structure of VgrG2bC-ter and confirm it is a member of the zinc-metallopeptidase family of enzymes. We show that this effector causes membrane blebbing at midcell, which suggests a distinct type of T6SS-mediated growth inhibition through interference with cell division, mimicking the impact of β-lactam antibiotics. Our study introduces a further effector family to the T6SS arsenal and demonstrates that VgrG2b can target both prokaryotic and eukaryotic cells. [Display omitted] •The structure of the VgrG2b C-terminal domain presents a metallopeptidase fold•VgrG2b exerts antibacterial activity in the periplasmic space•Toxicity of VgrG2b is counteracted by a cognate periplasmic immunity protein•VgrG2bC-ter-intoxicated prey cells bleb at the midcell and lyse The bacterial type VI secretion system (T6SS) delivers effector proteins into prokaryotic and eukaryotic cells to enhance the survival of the donor cell. Wood et al. describe an antibacterial T6SS toxin family eliciting a profound cell division defect and lysis. The structure of this periplasmic-acting toxin reveals a metallopeptidase fold.
Author Bullen, Nathan P.
Nolan, Laura M.
Howard, Sophie A.
Vollmer, Waldemar
Manoli, Eleni
Förster, Andreas
Hachani, Abderrahman
Hayward, Richard D.
Freemont, Paul S.
Filloux, Alain
Whitney, John C.
Yau, Hamish C.L.
Wood, Thomas E.
AuthorAffiliation 1 MRC Centre for Molecular Bacteriology and Infection, Department of Life Sciences, Imperial College London, London SW7 2AZ, UK
2 Section of Structural Biology, Department of Medicine, Imperial College London, London SW7 2AZ, UK
6 Division of Microbiology and Parasitology, Department of Pathology, University of Cambridge, Cambridge CB2 1QP, UK
5 Centre for Bacterial Cell Biology, Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle upon Tyne NE2 4HH, UK
3 Michael DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, ON L8S 4K1, Canada
4 Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, ON L8S 4L8, Canada
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31577948$$D View this record in MEDLINE/PubMed
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Tue Sep 17 21:19:30 EDT 2024
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Thu Sep 26 15:24:59 EDT 2024
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Wed May 17 00:05:52 EDT 2023
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Issue 1
Keywords Pseudomonas aeruginosa
effector
type VI secretion system
metallopeptidase
VgrG
Language English
License This is an open access article under the CC BY license.
Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
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Present address: DECTRIS Ltd., Täfernweg 1, 5405 Baden-Dättwil, Switzerland
Lead Contact
Present address: Department of Microbiology, Blavatnik Institute, Harvard Medical School, Boston, MA, USA
Present address: Department of Microbiology and Immunology, University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, VIC 3000, Australia
These authors contributed equally
Present address: Department of Pathogen Molecular Biology, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK
Present address: Department of Medicine, Division of Infectious Diseases, Massachusetts General Hospital, Boston, MA, USA
ORCID 0000-0003-1307-0289
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Snippet The type VI secretion system (T6SS) is crucial in interbacterial competition and is a virulence determinant of many Gram-negative bacteria. Several T6SS...
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SubjectTerms Anti-Bacterial Agents - pharmacology
Bacterial Proteins - metabolism
Bacterial Secretion Systems - metabolism
Bacterial Secretion Systems - physiology
beta-Lactams - metabolism
effector
metallopeptidase
Periplasm - drug effects
Periplasm - metabolism
Periplasm - physiology
Pseudomonas aeruginosa
Pseudomonas aeruginosa - drug effects
Pseudomonas aeruginosa - metabolism
Pseudomonas aeruginosa - physiology
type VI secretion system
Type VI Secretion Systems - metabolism
Type VI Secretion Systems - physiology
VgrG
Virulence Factors - metabolism
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Title The Pseudomonas aeruginosa T6SS Delivers a Periplasmic Toxin that Disrupts Bacterial Cell Morphology
URI https://dx.doi.org/10.1016/j.celrep.2019.08.094
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