Essential Role of the ESX-5 Secretion System in Outer Membrane Permeability of Pathogenic Mycobacteria

Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only present in slow-growing mycobacteria and responsible for the secretion of multiple substrates. However, the role of ESX-5 substrates in growth...

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Published inPLoS genetics Vol. 11; no. 5; p. e1005190
Main Authors Ates, Louis S, Ummels, Roy, Commandeur, Susanna, van de Weerd, Robert, van der Weerd, Robert, Sparrius, Marion, Weerdenburg, Eveline, Alber, Marina, Kalscheuer, Rainer, Piersma, Sander R, Abdallah, Abdallah M, Abd El Ghany, Moataz, Abdel-Haleem, Alyaa M, Pain, Arnab, Jiménez, Connie R, Bitter, Wilbert, Houben, Edith N G
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.05.2015
Public Library of Science (PLoS)
Subjects
Ampicillin - pharmacology
ATPases
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Bacteriology
Cell Membrane Permeability
Chromatography, Liquid
Data processing
DNA Transposable Elements
DNA, Bacterial - genetics
Drug Resistance, Bacterial
Experiments
Fatty acids
Gene expression
Gene Expression Regulation, Bacterial
Genetic aspects
Identification and classification
Lipids
Mutation
Mycobacteria
Mycobacterium bovis - genetics
Mycobacterium bovis - metabolism
Mycobacterium marinum - genetics
Mycobacterium marinum - metabolism
Mycobacterium tuberculosis - genetics
Mycobacterium tuberculosis - metabolism
Permeability
Physiological aspects
Protein binding
Proteins
Sequence Analysis, DNA
Tandem Mass Spectrometry
Tuberculosis
Type VII Secretion Systems - genetics
Type VII Secretion Systems - metabolism
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Abstract Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only present in slow-growing mycobacteria and responsible for the secretion of multiple substrates. However, the role of ESX-5 substrates in growth and/or virulence is largely unknown. In this study, we show that esx-5 is essential for growth of both Mycobacterium marinum and Mycobacterium bovis. Remarkably, this essentiality can be rescued by increasing the permeability of the outer membrane, either by altering its lipid composition or by the introduction of the heterologous porin MspA. Mutagenesis of the first nucleotide-binding domain of the membrane ATPase EccC5 prevented both ESX-5-dependent secretion and bacterial growth, but did not affect ESX-5 complex assembly. This suggests that the rescuing effect is not due to pores formed by the ESX-5 membrane complex, but caused by ESX-5 activity. Subsequent proteomic analysis to identify crucial ESX-5 substrates confirmed that all detectable PE and PPE proteins in the cell surface and cell envelope fractions were routed through ESX-5. Additionally, saturated transposon-directed insertion-site sequencing (TraDIS) was applied to both wild-type M. marinum cells and cells expressing mspA to identify genes that are not essential anymore in the presence of MspA. This analysis confirmed the importance of esx-5, but we could not identify essential ESX-5 substrates, indicating that multiple of these substrates are together responsible for the essentiality. Finally, examination of phenotypes on defined carbon sources revealed that an esx-5 mutant is strongly impaired in the uptake and utilization of hydrophobic carbon sources. Based on these data, we propose a model in which the ESX-5 system is responsible for the transport of cell envelope proteins that are required for nutrient uptake. These proteins might in this way compensate for the lack of MspA-like porins in slow-growing mycobacteria.
AbstractList Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only present in slow-growing mycobacteria and responsible for the secretion of multiple substrates. However, the role of ESX-5 substrates in growth and/or virulence is largely unknown. In this study, we show that esx-5 is essential for growth of both Mycobacterium marinum and Mycobacterium bovis. Remarkably, this essentiality can be rescued by increasing the permeability of the outer membrane, either by altering its lipid composition or by the introduction of the heterologous porin MspA. Mutagenesis of the first nucleotide-binding domain of the membrane ATPase EccC5 prevented both ESX-5-dependent secretion and bacterial growth, but did not affect ESX-5 complex assembly. This suggests that the rescuing effect is not due to pores formed by the ESX-5 membrane complex, but caused by ESX-5 activity. Subsequent proteomic analysis to identify crucial ESX-5 substrates confirmed that all detectable PE and PPE proteins in the cell surface and cell envelope fractions were routed through ESX-5. Additionally, saturated transposon-directed insertion-site sequencing (TraDIS) was applied to both wild-type M. marinum cells and cells expressing mspA to identify genes that are not essential anymore in the presence of MspA. This analysis confirmed the importance of esx-5, but we could not identify essential ESX-5 substrates, indicating that multiple of these substrates are together responsible for the essentiality. Finally, examination of phenotypes on defined carbon sources revealed that an esx-5 mutant is strongly impaired in the uptake and utilization of hydrophobic carbon sources. Based on these data, we propose a model in which the ESX-5 system is responsible for the transport of cell envelope proteins that are required for nutrient uptake. These proteins might in this way compensate for the lack of MspA-like porins in slow-growing mycobacteria.
Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only present in slow-growing mycobacteria and responsible for the secretion of multiple substrates. However, the role of ESX-5 substrates in growth and/or virulence is largely unknown. In this study, we show that esx-5 is essential for growth of both Mycobacterium marinum and Mycobacterium bovis. Remarkably, this essentiality can be rescued by increasing the permeability of the outer membrane, either by altering its lipid composition or by the introduction of the heterologous porin MspA. Mutagenesis of the first nucleotide-binding domain of the membrane ATPase [EccC.sub.5] prevented both ESX-5-dependent secretion and bacterial growth, but did not affect ESX-5 complex assembly. This suggests that the rescuing effect is not due to pores formed by the ESX-5 membrane complex, but caused by ESX-5 activity. Subsequent proteomic analysis to identify crucial ESX-5 substrates confirmed that all detectable PE and PPE proteins in the cell surface and cell envelope fractions were routed through ESX-5. Additionally, saturated transposon-directed insertion-site sequencing (TraDIS) was applied to both wild-type M. marinum cells and cells expressing mspA to identify genes that are not essential anymore in the presence of MspA. This analysis confirmed the importance of esx-5, but we could not identify essential ESX-5 substrates, indicating that multiple of these substrates are together responsible for the essentiality. Finally, examination of phenotypes on defined carbon sources revealed that an esx-5 mutant is strongly impaired in the uptake and utilization of hydrophobic carbon sources. Based on these data, we propose a model in which the ESX-5 system is responsible for the transport of cell envelope proteins that are required for nutrient uptake. These proteins might in this way compensate for the lack of MspA-like porins in slow-growing mycobacteria.
  Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only present in slow-growing mycobacteria and responsible for the secretion of multiple substrates. However, the role of ESX-5 substrates in growth and/or virulence is largely unknown. In this study, we show that esx-5 is essential for growth of both Mycobacterium marinum and Mycobacterium bovis. Remarkably, this essentiality can be rescued by increasing the permeability of the outer membrane, either by altering its lipid composition or by the introduction of the heterologous porin MspA. Mutagenesis of the first nucleotide-binding domain of the membrane ATPase EccC5 prevented both ESX-5-dependent secretion and bacterial growth, but did not affect ESX-5 complex assembly. This suggests that the rescuing effect is not due to pores formed by the ESX-5 membrane complex, but caused by ESX-5 activity. Subsequent proteomic analysis to identify crucial ESX-5 substrates confirmed that all detectable PE and PPE proteins in the cell surface and cell envelope fractions were routed through ESX-5. Additionally, saturated transposon-directed insertion-site sequencing (TraDIS) was applied to both wild-type M. marinum cells and cells expressing mspA to identify genes that are not essential anymore in the presence of MspA. This analysis confirmed the importance of esx-5, but we could not identify essential ESX-5 substrates, indicating that multiple of these substrates are together responsible for the essentiality. Finally, examination of phenotypes on defined carbon sources revealed that an esx-5 mutant is strongly impaired in the uptake and utilization of hydrophobic carbon sources. Based on these data, we propose a model in which the ESX-5 system is responsible for the transport of cell envelope proteins that are required for nutrient uptake. These proteins might in this way compensate for the lack of MspA-like porins in slow-growing mycobacteria.
Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only present in slow-growing mycobacteria and responsible for the secretion of multiple substrates. However, the role of ESX-5 substrates in growth and/or virulence is largely unknown. In this study, we show that esx-5 is essential for growth of both Mycobacterium marinum and Mycobacterium bovis . Remarkably, this essentiality can be rescued by increasing the permeability of the outer membrane, either by altering its lipid composition or by the introduction of the heterologous porin MspA. Mutagenesis of the first nucleotide-binding domain of the membrane ATPase EccC 5 prevented both ESX-5-dependent secretion and bacterial growth, but did not affect ESX-5 complex assembly. This suggests that the rescuing effect is not due to pores formed by the ESX-5 membrane complex, but caused by ESX-5 activity. Subsequent proteomic analysis to identify crucial ESX-5 substrates confirmed that all detectable PE and PPE proteins in the cell surface and cell envelope fractions were routed through ESX-5. Additionally, saturated transposon-directed insertion-site sequencing (TraDIS) was applied to both wild-type M . marinum cells and cells expressing mspA to identify genes that are not essential anymore in the presence of MspA. This analysis confirmed the importance of esx-5 , but we could not identify essential ESX-5 substrates, indicating that multiple of these substrates are together responsible for the essentiality. Finally, examination of phenotypes on defined carbon sources revealed that an esx-5 mutant is strongly impaired in the uptake and utilization of hydrophobic carbon sources. Based on these data, we propose a model in which the ESX-5 system is responsible for the transport of cell envelope proteins that are required for nutrient uptake. These proteins might in this way compensate for the lack of MspA-like porins in slow-growing mycobacteria. Mycobacteria have a thick protective outer membrane that helps them to withstand adverse conditions both outside and within the host. However, in order to cause disease, the bacterium also needs to secrete proteins across this outer membrane. To achieve this, mycobacteria possess so-called type VII secretion systems. One of these systems, the ESX-5 secretion system, is only present in the group of slow-growing mycobacteria, which contains most pathogenic species. In this study, we show that the ESX-5 system is essential for growth of mycobacteria. We found that when we generated a ‘leaky’ outer membrane, by interfering in the construction of the outer membrane, or by introducing an outer membrane porin, the ESX-5 system was no longer essential for growth. We additionally show that ESX-5 mediates uptake of fatty acids, which suggests that ESX-5 substrates can form specific transport systems or pores in the outer membrane required for the uptake of crucial nutrients. Understanding the role of ESX-5 in outer membrane permeability helps us to understand a fundamental difference between fast-growing and slow-growing mycobacteria. Since most pathogenic mycobacteria are slow-growing this helps us to understand the mycobacterial requirements for pathogenesis in more detail.
Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only present in slow-growing mycobacteria and responsible for the secretion of multiple substrates. However, the role of ESX-5 substrates in growth and/or virulence is largely unknown. In this study, we show that esx-5 is essential for growth of both Mycobacterium marinum and Mycobacterium bovis. Remarkably, this essentiality can be rescued by increasing the permeability of the outer membrane, either by altering its lipid composition or by the introduction of the heterologous porin MspA. Mutagenesis of the first nucleotide-binding domain of the membrane ATPase EccC5 prevented both ESX-5-dependent secretion and bacterial growth, but did not affect ESX-5 complex assembly. This suggests that the rescuing effect is not due to pores formed by the ESX-5 membrane complex, but caused by ESX-5 activity. Subsequent proteomic analysis to identify crucial ESX-5 substrates confirmed that all detectable PE and PPE proteins in the cell surface and cell envelope fractions were routed through ESX-5. Additionally, saturated transposon-directed insertion-site sequencing (TraDIS) was applied to both wild-type M. marinum cells and cells expressing mspA to identify genes that are not essential anymore in the presence of MspA. This analysis confirmed the importance of esx-5, but we could not identify essential ESX-5 substrates, indicating that multiple of these substrates are together responsible for the essentiality. Finally, examination of phenotypes on defined carbon sources revealed that an esx-5 mutant is strongly impaired in the uptake and utilization of hydrophobic carbon sources. Based on these data, we propose a model in which the ESX-5 system is responsible for the transport of cell envelope proteins that are required for nutrient uptake. These proteins might in this way compensate for the lack of MspA-like porins in slow-growing mycobacteria.Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only present in slow-growing mycobacteria and responsible for the secretion of multiple substrates. However, the role of ESX-5 substrates in growth and/or virulence is largely unknown. In this study, we show that esx-5 is essential for growth of both Mycobacterium marinum and Mycobacterium bovis. Remarkably, this essentiality can be rescued by increasing the permeability of the outer membrane, either by altering its lipid composition or by the introduction of the heterologous porin MspA. Mutagenesis of the first nucleotide-binding domain of the membrane ATPase EccC5 prevented both ESX-5-dependent secretion and bacterial growth, but did not affect ESX-5 complex assembly. This suggests that the rescuing effect is not due to pores formed by the ESX-5 membrane complex, but caused by ESX-5 activity. Subsequent proteomic analysis to identify crucial ESX-5 substrates confirmed that all detectable PE and PPE proteins in the cell surface and cell envelope fractions were routed through ESX-5. Additionally, saturated transposon-directed insertion-site sequencing (TraDIS) was applied to both wild-type M. marinum cells and cells expressing mspA to identify genes that are not essential anymore in the presence of MspA. This analysis confirmed the importance of esx-5, but we could not identify essential ESX-5 substrates, indicating that multiple of these substrates are together responsible for the essentiality. Finally, examination of phenotypes on defined carbon sources revealed that an esx-5 mutant is strongly impaired in the uptake and utilization of hydrophobic carbon sources. Based on these data, we propose a model in which the ESX-5 system is responsible for the transport of cell envelope proteins that are required for nutrient uptake. These proteins might in this way compensate for the lack of MspA-like porins in slow-growing mycobacteria.
Audience Academic
Author Kalscheuer, Rainer
Pain, Arnab
van der Weerd, Robert
Commandeur, Susanna
Houben, Edith N G
Jiménez, Connie R
Sparrius, Marion
Piersma, Sander R
van de Weerd, Robert
Weerdenburg, Eveline
Abd El Ghany, Moataz
Ates, Louis S
Alber, Marina
Abdallah, Abdallah M
Ummels, Roy
Abdel-Haleem, Alyaa M
Bitter, Wilbert
AuthorAffiliation 4 Biological and Environmental Sciences and Engineering (BESE) division, King Abdullah University of Science and Technology (KAUST), Thuwal, Kingdom of Saudi Arabia
University of Geneva Medical School, SWITZERLAND
5 Section Molecular Microbiology, Amsterdam Institute of Molecules, Medicine & Systems, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands
3 Department of Medical Oncology, OncoProteomics Laboratory, VU University Medical Center, Amsterdam, the Netherlands
1 Department of Medical Microbiology and Infection Control, VU University Medical Center, Amsterdam, the Netherlands
2 Institute for Medical Microbiology and Hospital Hygiene, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany
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– name: 2 Institute for Medical Microbiology and Hospital Hygiene, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany
– name: 4 Biological and Environmental Sciences and Engineering (BESE) division, King Abdullah University of Science and Technology (KAUST), Thuwal, Kingdom of Saudi Arabia
– name: University of Geneva Medical School, SWITZERLAND
– name: 3 Department of Medical Oncology, OncoProteomics Laboratory, VU University Medical Center, Amsterdam, the Netherlands
– name: 5 Section Molecular Microbiology, Amsterdam Institute of Molecules, Medicine & Systems, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands
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  organization: Section Molecular Microbiology, Amsterdam Institute of Molecules, Medicine & Systems, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25938982$$D View this record in MEDLINE/PubMed
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The authors have declared that no competing interests exist.
Conceived and designed the experiments: LSA RU SC EW AMA RK SRP WB ENGH. Performed the experiments: LSA RU SC RvdW MAEG AMAH MS MA SRP ENGH. Analyzed the data: LSA SC RK SRP AMA AMAH WB ENGH. Contributed reagents/materials/analysis tools: RK AP CRJ. Wrote the paper: LSA RU SC RvdW AMA RK SRP WB ENGH.
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Snippet Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only...
  Mycobacteria possess different type VII secretion (T7S) systems to secrete proteins across their unusual cell envelope. One of these systems, ESX-5, is only...
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StartPage e1005190
SubjectTerms Ampicillin - pharmacology
ATPases
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Bacteriology
Cell Membrane Permeability
Chromatography, Liquid
Data processing
DNA Transposable Elements
DNA, Bacterial - genetics
Drug Resistance, Bacterial
Experiments
Fatty acids
Gene expression
Gene Expression Regulation, Bacterial
Genetic aspects
Identification and classification
Lipids
Mutation
Mycobacteria
Mycobacterium bovis - genetics
Mycobacterium bovis - metabolism
Mycobacterium marinum - genetics
Mycobacterium marinum - metabolism
Mycobacterium tuberculosis - genetics
Mycobacterium tuberculosis - metabolism
Permeability
Physiological aspects
Protein binding
Proteins
Sequence Analysis, DNA
Tandem Mass Spectrometry
Tuberculosis
Type VII Secretion Systems - genetics
Type VII Secretion Systems - metabolism
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Title Essential Role of the ESX-5 Secretion System in Outer Membrane Permeability of Pathogenic Mycobacteria
URI https://www.ncbi.nlm.nih.gov/pubmed/25938982
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http://dx.doi.org/10.1371/journal.pgen.1005190
Volume 11
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