Envelope stress responses defend against type six secretion system attacks independently of immunity proteins
The arms race among microorganisms is a key driver in the evolution of not only the weapons but also defence mechanisms. Many Gram-negative bacteria use the type six secretion system (T6SS) to deliver toxic effectors directly into neighbouring cells. Defence against effectors requires cognate immuni...
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Published in | Nature microbiology Vol. 5; no. 5; pp. 706 - 714 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
01.05.2020
Nature Publishing Group |
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Abstract | The arms race among microorganisms is a key driver in the evolution of not only the weapons but also defence mechanisms. Many Gram-negative bacteria use the type six secretion system (T6SS) to deliver toxic effectors directly into neighbouring cells. Defence against effectors requires cognate immunity proteins. However, here we show immunity-independent protection mediated by envelope stress responses in
Escherichia coli
and
Vibrio cholerae
against a
V. cholerae
T6SS effector, TseH. We demonstrate that TseH is a PAAR-dependent species-specific effector highly potent against
Aeromonas
species but not against its
V. cholerae
immunity mutant or
E. coli
. A structural analysis reveals TseH is probably a NlpC/P60-family cysteine endopeptidase. We determine that two envelope stress-response pathways, Rcs and BaeSR, protect
E. coli
from TseH toxicity by mechanisms including capsule synthesis. The two-component system WigKR (VxrAB) is critical for protecting
V. cholerae
from its own T6SS despite expressing immunity genes. WigR also regulates T6SS expression, suggesting a dual role in attack and defence. This deepens our understanding of how bacteria survive T6SS attacks and suggests that defence against the T6SS represents a major selective pressure driving the evolution of species-specific effectors and protective mechanisms mediated by envelope stress responses and capsule synthesis.
Defence against type six secretion system (T6SS) effectors is thought to be mostly mediated by dedicated immunity proteins that antagonize specific effector proteins. Here, two envelope stress-response pathways, Rcs and BaeSR, are shown to regulate protection against the T6SS effector TseH by modulating the integrity of the bacterial envelope in a manner independent of immunity proteins. |
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AbstractList | The arms race among microorganisms is a key driver in the evolution of not only the weapons but also defence mechanisms. Many Gram-negative bacteria use the type six secretion system (T6SS) to deliver toxic effectors directly into neighbouring cells. Defence against effectors requires cognate immunity proteins. However, here we show immunity-independent protection mediated by envelope stress responses in Escherichia coli and Vibrio cholerae against a V. cholerae T6SS effector, TseH. We demonstrate that TseH is a PAAR-dependent species-specific effector highly potent against Aeromonas species but not against its V. cholerae immunity mutant or E. coli. A structural analysis reveals TseH is probably a NlpC/P60-family cysteine endopeptidase. We determine that two envelope stress-response pathways, Rcs and BaeSR, protect E. coli from TseH toxicity by mechanisms including capsule synthesis. The two-component system WigKR (VxrAB) is critical for protecting V. cholerae from its own T6SS despite expressing immunity genes. WigR also regulates T6SS expression, suggesting a dual role in attack and defence. This deepens our understanding of how bacteria survive T6SS attacks and suggests that defence against the T6SS represents a major selective pressure driving the evolution of species-specific effectors and protective mechanisms mediated by envelope stress responses and capsule synthesis. The arms race among microorganisms is a key driver in the evolution of not only the weapons but also defence mechanisms. Many Gram-negative bacteria use the type six secretion system (T6SS) to deliver toxic effectors directly into neighbouring cells. Defence against effectors requires cognate immunity proteins. However, here we show immunity-independent protection mediated by envelope stress responses in Escherichia coli and Vibrio cholerae against a V. cholerae T6SS effector, TseH. We demonstrate that TseH is a PAAR-dependent species-specific effector highly potent against Aeromonas species but not against its V. cholerae immunity mutant or E. coli . A structural analysis reveals TseH is probably a NlpC/P60-family cysteine endopeptidase. We determine that two envelope stress-response pathways, Rcs and BaeSR, protect E. coli from TseH toxicity by mechanisms including capsule synthesis. The two-component system WigKR (VxrAB) is critical for protecting V. cholerae from its own T6SS despite expressing immunity genes. WigR also regulates T6SS expression, suggesting a dual role in attack and defence. This deepens our understanding of how bacteria survive T6SS attacks and suggests that defence against the T6SS represents a major selective pressure driving the evolution of species-specific effectors and protective mechanisms mediated by envelope stress responses and capsule synthesis. Defence against type six secretion system (T6SS) effectors is thought to be mostly mediated by dedicated immunity proteins that antagonize specific effector proteins. Here, two envelope stress-response pathways, Rcs and BaeSR, are shown to regulate protection against the T6SS effector TseH by modulating the integrity of the bacterial envelope in a manner independent of immunity proteins. The arms race among microbes is a key driver in the evolution of not only the weapons but also defence mechanisms. Many gram-negative bacteria use the type six secretion system (T6SS) to deliver toxic effectors directly into neighbouring cells. Defence against effectors requires cognate immunity proteins. However, here we show immunity-independent protection mediated by envelope stress responses in Escherichia coli and Vibrio cholerae against a V. cholerae T6SS effector, TseH. We demonstrate that TseH is a PAAR-dependent species-specific effector highly potent against Aeromonas species but not against its V. cholerae immunity mutant or E. coli . Structural analysis reveals TseH is likely a NlpC/P60 family cysteine endopeptidase. We determine that two envelope stress response pathways, Rcs and BaeSR, protect E. coli from TseH toxicity by mechanisms including capsule synthesis. The two-component system WigKR (VxrAB) is critical for protecting V. cholerae from its own T6SS despite expressing immunity genes. WigR also regulates T6SS expression, suggesting a dual role in attack and defence. This deepens our understanding of how bacteria survive T6SS attacks and suggests that defending against the T6SS represents a major selective pressure driving the evolution of species-specific effectors and protective mechanisms mediated by envelope stress responses and capsule synthesis. The arms race among microorganisms is a key driver in the evolution of not only the weapons but also defence mechanisms. Many Gram-negative bacteria use the type six secretion system (T6SS) to deliver toxic effectors directly into neighbouring cells. Defence against effectors requires cognate immunity proteins. However, here we show immunity-independent protection mediated by envelope stress responses in Escherichia coli and Vibrio cholerae against a V. cholerae T6SS effector, TseH. We demonstrate that TseH is a PAAR-dependent species-specific effector highly potent against Aeromonas species but not against its V. cholerae immunity mutant or E. coli. A structural analysis reveals TseH is probably a NlpC/P60-family cysteine endopeptidase. We determine that two envelope stress-response pathways, Rcs and BaeSR, protect E. coli from TseH toxicity by mechanisms including capsule synthesis. The two-component system WigKR (VxrAB) is critical for protecting V. cholerae from its own T6SS despite expressing immunity genes. WigR also regulates T6SS expression, suggesting a dual role in attack and defence. This deepens our understanding of how bacteria survive T6SS attacks and suggests that defence against the T6SS represents a major selective pressure driving the evolution of species-specific effectors and protective mechanisms mediated by envelope stress responses and capsule synthesis.Defence against type six secretion system (T6SS) effectors is thought to be mostly mediated by dedicated immunity proteins that antagonize specific effector proteins. Here, two envelope stress-response pathways, Rcs and BaeSR, are shown to regulate protection against the T6SS effector TseH by modulating the integrity of the bacterial envelope in a manner independent of immunity proteins. |
Author | Dong, Tao G. Manera, Kevin Lam, Linh Burkinshaw, Brianne Watanabe, Nobuhiko Hersch, Steven J. Kamal, Fatima Savchenko, Alexei Stietz, Maria Silvina Li, Meixin Pun, Alexander |
AuthorAffiliation | 2, Department of Microbiology, Immunology and Infectious Diseases, University of Calgary, Calgary, Canada 1, Department of Ecosystem and Public Health, University of Calgary, Calgary, Canada 3, State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, China |
AuthorAffiliation_xml | – name: 1, Department of Ecosystem and Public Health, University of Calgary, Calgary, Canada – name: 3, State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, China – name: 2, Department of Microbiology, Immunology and Infectious Diseases, University of Calgary, Calgary, Canada |
Author_xml | – sequence: 1 givenname: Steven J. orcidid: 0000-0001-6186-0133 surname: Hersch fullname: Hersch, Steven J. organization: Department of Ecosystem and Public Health, University of Calgary – sequence: 2 givenname: Nobuhiko surname: Watanabe fullname: Watanabe, Nobuhiko organization: Department of Microbiology, Immunology and Infectious Diseases, University of Calgary – sequence: 3 givenname: Maria Silvina surname: Stietz fullname: Stietz, Maria Silvina organization: Department of Ecosystem and Public Health, University of Calgary – sequence: 4 givenname: Kevin surname: Manera fullname: Manera, Kevin organization: Department of Ecosystem and Public Health, University of Calgary – sequence: 5 givenname: Fatima surname: Kamal fullname: Kamal, Fatima organization: Department of Ecosystem and Public Health, University of Calgary – sequence: 6 givenname: Brianne surname: Burkinshaw fullname: Burkinshaw, Brianne organization: Department of Ecosystem and Public Health, University of Calgary – sequence: 7 givenname: Linh surname: Lam fullname: Lam, Linh organization: Department of Ecosystem and Public Health, University of Calgary – sequence: 8 givenname: Alexander surname: Pun fullname: Pun, Alexander organization: Department of Ecosystem and Public Health, University of Calgary – sequence: 9 givenname: Meixin surname: Li fullname: Li, Meixin organization: Department of Ecosystem and Public Health, University of Calgary – sequence: 10 givenname: Alexei surname: Savchenko fullname: Savchenko, Alexei organization: Department of Microbiology, Immunology and Infectious Diseases, University of Calgary – sequence: 11 givenname: Tao G. orcidid: 0000-0003-3557-1850 surname: Dong fullname: Dong, Tao G. email: tdong@ucalgary.ca organization: Department of Ecosystem and Public Health, University of Calgary, State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic and Developmental Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32094588$$D View this record in MEDLINE/PubMed |
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Notes | S.J.H. designed, performed and analysed most of the biological experiments and prepared the manuscript and figures. N.W. and A.S. performed and analysed the crystallography. M.S.S. performed the microscopy. K.M. performed and analysed the RT-qPCR. F.K. performed the permeability analysis, helped construct plasmids and identified reduced toxicity TseH mutants. B.B. performed and analyzed the pull-down assays. L.L. analysed genome sequencing data. A.P. and M.L. helped construct strains and plasmids. N.W., A.S. and T.G.D. contributed to manuscript revision. T.G.D. conceived the project and supervised the study. Author contributions |
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Snippet | The arms race among microorganisms is a key driver in the evolution of not only the weapons but also defence mechanisms. Many Gram-negative bacteria use the... The arms race among microbes is a key driver in the evolution of not only the weapons but also defence mechanisms. Many gram-negative bacteria use the type six... |
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SubjectTerms | 14/63 38/90 45/77 631/326/2565 631/326/41/2180 631/326/41/2482 631/326/41/2529 82/80 82/83 Bacterial Proteins - genetics Bacterial Proteins - metabolism Biomedical and Life Sciences Defense E coli Endopeptidase Escherichia coli - genetics Escherichia coli - metabolism Gene Expression Regulation, Bacterial Gram-negative bacteria Immunity - genetics Infectious Diseases Life Sciences Medical Microbiology Microbiology Models, Molecular Parasitology Protein Conformation Proteins Species Toxicity Type VI Secretion Systems - chemistry Type VI Secretion Systems - genetics Type VI Secretion Systems - immunology Type VI Secretion Systems - metabolism Vibrio cholerae - genetics Vibrio cholerae - metabolism Virology Virulence - genetics |
Title | Envelope stress responses defend against type six secretion system attacks independently of immunity proteins |
URI | https://link.springer.com/article/10.1038/s41564-020-0672-6 https://www.ncbi.nlm.nih.gov/pubmed/32094588 https://www.proquest.com/docview/2395249626 https://www.proquest.com/docview/2475023819 https://pubmed.ncbi.nlm.nih.gov/PMC7190449 |
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