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

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    Type
    Article
    Authors
    Ates, Louis S. cc
    Ummels, Roy
    Commandeur, Susanna
    van der Weerd, Robert
    Sparrius, Marion
    Weerdenburg, Eveline
    Alber, Marina
    Kalscheuer, Rainer
    Piersma, Sander R.
    Abdallah, Abdallah
    Abd El Ghany, Moataz
    Abdel-Haleem, Alyaa M. cc
    Pain, Arnab cc
    Jiménez, Connie R.
    Bitter, Wilbert cc
    Houben, Edith N.G.
    KAUST Department
    Biological and Environmental Sciences and Engineering (BESE) Division
    Bioscience Program
    Date
    2015-05-04
    Permanent link to this record
    http://hdl.handle.net/10754/552778
    
    Metadata
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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.
    Citation
    Essential Role of the ESX-5 Secretion System in Outer Membrane Permeability of Pathogenic Mycobacteria 2015, 11 (5):e1005190 PLOS Genetics
    Publisher
    Public Library of Science (PLoS)
    Journal
    PLOS Genetics
    DOI
    10.1371/journal.pgen.1005190
    PubMed ID
    25938982
    PubMed Central ID
    PMC4418733
    Additional Links
    http://dx.plos.org/10.1371/journal.pgen.1005190
    ae974a485f413a2113503eed53cd6c53
    10.1371/journal.pgen.1005190
    Scopus Count
    Collections
    Articles; Biological and Environmental Sciences and Engineering (BESE) Division; Bioscience Program

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