1887

Abstract

Successful occupancy of a given niche requires the colonising bacteria to interact extensively with the biotic and abiotic environment, including other resident microbes. Bacteria have evolved a range of protein secretion machines for this purpose with eleven such systems identified to date. The type VIIb secretion system (T7SSb) is utilised by Bacillota to secrete a range of protein substrates, including antibacterial toxins targeting closely related strains, and the system as a whole has been implicated in a range of activities such as iron acquisition, intercellular signalling, host colonisation and virulence. This review covers the components and secretion mechanism of the T7SSb, the substrates of these systems and their roles in Gram-positive bacteria, with a focus on interbacterial competition.

Funding
This study was supported by the:
  • Wellcome Trust (Award 224151/Z/21/Z)
    • Principle Award Recipient: TracyPalmer
  • Wellcome Trust (Award 10183/Z/15/Z)
    • Principle Award Recipient: TracyPalmer
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001420
2023-12-20
2024-07-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/169/12/mic001420.html?itemId=/content/journal/micro/10.1099/mic.0.001420&mimeType=html&fmt=ahah

References

  1. Filloux A. Bacterial protein secretion systems: game of types. Microbiology 2022; 168:001193 [View Article] [PubMed]
    [Google Scholar]
  2. Bansal-Mutalik R, Nikaido H. Mycobacterial outer membrane is a lipid bilayer and the inner membrane is unusually rich in diacyl phosphatidylinositol dimannosides. Proc Natl Acad Sci U S A 2014; 111:4958–4963 [View Article] [PubMed]
    [Google Scholar]
  3. Sørensen AL, Nagai S, Houen G, Andersen P, Andersen AB. Purification and characterization of a low-molecular-mass T-cell antigen secreted by Mycobacterium tuberculosis. Infect Immun 1995; 63:1710–1717 [View Article] [PubMed]
    [Google Scholar]
  4. Andersen P, Andersen AB, Sørensen AL, Nagai S. Recall of long-lived immunity to Mycobacterium tuberculosis infection in mice. J Immunol 1995; 154:3359–3372 [PubMed]
    [Google Scholar]
  5. Pallen MJ. The ESAT-6/WXG100 superfamily -- and a new gram-positive secretion system?. Trends Microbiol 2002; 10:209–212 [View Article] [PubMed]
    [Google Scholar]
  6. Hsu T, Hingley-Wilson SM, Chen B, Chen M, Dai AZ et al. The primary mechanism of attenuation of bacillus calmette-guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci U S A 2003; 100:12420–12425 [View Article] [PubMed]
    [Google Scholar]
  7. Pym AS, Brodin P, Brosch R, Huerre M, Cole ST. Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 2002; 46:709–717 [View Article] [PubMed]
    [Google Scholar]
  8. Stanley SA, Raghavan S, Hwang WW, Cox JS. Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc Natl Acad Sci U S A 2003; 100:13001–13006 [View Article] [PubMed]
    [Google Scholar]
  9. Chirakos AE, Balaram A, Conrad W, Champion PA. Modeling tubercular ESX-1 secretion using Mycobacterium marinum. Microbiol Mol Biol Rev 2020; 84:e00082-19 [View Article] [PubMed]
    [Google Scholar]
  10. Bunduc CM, Bitter W, Houben ENG. Structure and function of the mycobacterial Type VII secretion systems. Annu Rev Microbiol 2020; 74:315–335 [View Article] [PubMed]
    [Google Scholar]
  11. Burts ML, Williams WA, DeBord K, Missiakas DM. EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. Proc Natl Acad Sci U S A 2005; 102:1169–1174 [View Article] [PubMed]
    [Google Scholar]
  12. Sysoeva TA, Zepeda-Rivera MA, Huppert LA, Burton BM. Dimer recognition and secretion by the ESX secretion system in Bacillus subtilis. Proc Natl Acad Sci U S A 2014; 111:7653–7658 [View Article] [PubMed]
    [Google Scholar]
  13. Huppert LA, Ramsdell TL, Chase MR, Sarracino DA, Fortune SM et al. The ESX system in Bacillus subtilis mediates protein secretion. PLoS One 2014; 9:e96267 [View Article] [PubMed]
    [Google Scholar]
  14. Sun Z, Zhou D, Zhang X, Li Q, Lin H et al. Determining the genetic characteristics of resistance and virulence of the “Epidermidis Cluster Group” through pan-genome analysis. Front Cell Infect Microbiol 2020; 10:274 [View Article] [PubMed]
    [Google Scholar]
  15. Warne B, Harkins CP, Harris SR, Vatsiou A, Stanley-Wall N et al. The Ess/Type VII secretion system of Staphylococcus aureus shows unexpected genetic diversity. BMC Genomics 2016; 17:222 [View Article] [PubMed]
    [Google Scholar]
  16. Spencer BL, Tak U, Mendonça JC, Nagao PE, Niederweis M et al. A type VII secretion system in group B Streptococcus mediates cytotoxicity and virulence. PLoS Pathog 2021; 17:e1010121 [View Article] [PubMed]
    [Google Scholar]
  17. Teh WK, Ding Y, Gubellini F, Filloux A, Poyart C et al. Characterization of TelE, a T7SS LXG effector exhibiting a conserved C-terminal glycine zipper motif required for toxicity. Microbiol Spectr 2023; 11:e01481-23 [View Article] [PubMed]
    [Google Scholar]
  18. Garufi G, Butler E, Missiakas D. ESAT-6-like protein secretion in Bacillus anthracis. J Bacteriol 2008; 190:7004–7011 [View Article] [PubMed]
    [Google Scholar]
  19. Chatterjee A, Willett JLE, Nguyen UT, Monogue B, Palmer KL et al. Parallel genomics uncover novel enterococcal-bacteriophage interactions. mBio 2020; 11:e03120-19 [View Article] [PubMed]
    [Google Scholar]
  20. Bowran K, Palmer T. Extreme genetic diversity in the type VII secretion system of Listeria monocytogenes suggests a role in bacterial antagonism. Microbiology 2021; 167:001034 [View Article] [PubMed]
    [Google Scholar]
  21. Poulsen C, Panjikar S, Holton SJ, Wilmanns M, Song Y-H. WXG100 protein superfamily consists of three subfamilies and exhibits an α-helical C-terminal conserved residue pattern. PLoS One 2014; 9:e89313 [View Article] [PubMed]
    [Google Scholar]
  22. Sutcliffe IC. New insights into the distribution of WXG100 protein secretion systems. Antonie van Leeuwenhoek 2011; 99:127–131 [View Article] [PubMed]
    [Google Scholar]
  23. Unnikrishnan M, Constantinidou C, Palmer T, Pallen MJ. The enigmatic Esx proteins: looking beyond mycobacteria. Trends Microbiol 2017; 25:192–204 [View Article] [PubMed]
    [Google Scholar]
  24. Champion PAD, Stanley SA, Champion MM, Brown EJ, Cox JS. C-terminal signal sequence promotes virulence factor secretion in Mycobacterium tuberculosis. Science 2006; 313:1632–1636 [View Article] [PubMed]
    [Google Scholar]
  25. Rivera-Calzada A, Famelis N, Llorca O, Geibel S. Type VII secretion systems: structure, functions and transport models. Nat Rev Microbiol 2021; 19:567–584 [View Article] [PubMed]
    [Google Scholar]
  26. Sundaramoorthy R, Fyfe PK, Hunter WN. Structure of Staphylococcus aureus EsxA suggests a contribution to virulence by action as a transport chaperone and/or adaptor protein. J Mol Biol 2008; 383:603–614 [View Article] [PubMed]
    [Google Scholar]
  27. Shukla A, Pallen M, Anthony M, White SA. The homodimeric GBS1074 from Streptococcus agalactiae. Acta Cryst F 2010; 66:1421–1425 [View Article] [PubMed]
    [Google Scholar]
  28. Zoltner M, Ng W, Money JJ, Fyfe PK, Kneuper H et al. EssC: domain structures inform on the elusive translocation channel in the Type VII secretion system. Biochem J 2016; 473:1941–1952 [View Article] [PubMed]
    [Google Scholar]
  29. Bunduc CM, Fahrenkamp D, Wald J, Ummels R, Bitter W et al. Structure and dynamics of a mycobacterial type VII secretion system. Nature 2021; 593:445–448 [View Article] [PubMed]
    [Google Scholar]
  30. Beckham KSH, Ritter C, Chojnowski G, Ziemianowicz DS, Mullapudi E et al. Structure of the mycobacterial ESX-5 type VII secretion system pore complex. Sci Adv 2021; 7:eabg9923 [View Article] [PubMed]
    [Google Scholar]
  31. Famelis N, Rivera-Calzada A, Degliesposti G, Wingender M, Mietrach N et al. Architecture of the mycobacterial type VII secretion system. Nature 2019; 576:321–325 [View Article] [PubMed]
    [Google Scholar]
  32. Chen Y-H, Anderson M, Hendrickx APA, Missiakas D. Characterization of EssB, a protein required for secretion of ESAT-6 like proteins in Staphylococcus aureus. BMC Microbiol 2012; 12:219 [View Article] [PubMed]
    [Google Scholar]
  33. Kneuper H, Cao ZP, Twomey KB, Zoltner M, Jäger F et al. Heterogeneity in ess transcriptional organization and variable contribution of the Ess/Type VII protein secretion system to virulence across closely related Staphylocccus aureus strains. Mol Microbiol 2014; 93:928–943 [View Article] [PubMed]
    [Google Scholar]
  34. Taylor JC, Gao X, Xu J, Holder M, Petrosino J et al. A type VII secretion system of Streptococcus gallolyticus subsp. gallolyticus contributes to gut colonization and the development of colon tumors. PLoS Pathog 2021; 17:e1009182 [View Article] [PubMed]
    [Google Scholar]
  35. Spencer BL, Job AM, Robertson CM, Hameed ZA, Serchejian C et al. Heterogeneity of the group B streptococcal type VII secretion system and influence on colonization of the female genital tract. Mol Microbiol 2023; 120:258–275 [View Article] [PubMed]
    [Google Scholar]
  36. Schindler Y, Rahav G, Nissan I, Valenci G, Ravins M et al. Type VII secretion system and its effect on group B Streptococcus virulence in isolates obtained from newborns with early onset disease and colonized pregnant women. Front Cell Infect Microbiol 2023; 13:1168530 [View Article] [PubMed]
    [Google Scholar]
  37. Rosenberg OS, Dovala D, Li X, Connolly L, Bendebury A et al. Substrates control multimerization and activation of the multi-domain ATPase motor of type VII secretion. Cell 2015; 161:501–512 [View Article] [PubMed]
    [Google Scholar]
  38. Mietrach N, Damián-Aparicio D, Mielich-Süss B, Lopez D, Geibel S. Substrate interaction with the EssC coupling protein of the type VIIb secretion system. J Bacteriol 2020; 202:e00646-19 [View Article] [PubMed]
    [Google Scholar]
  39. Ramsdell TL, Huppert LA, Sysoeva TA, Fortune SM, Burton BM. Linked domain architectures allow for specialization of function in the FtsK/SpoIIIE ATPases of ESX secretion systems. J Mol Biol 2015; 427:1119–1132 [View Article] [PubMed]
    [Google Scholar]
  40. Tanaka Y, Kuroda M, Yasutake Y, Yao M, Tsumoto K et al. Crystal structure analysis reveals a novel forkhead-associated domain of ESAT-6 secretion system C protein in Staphylococcus aureus. Proteins: Struct Funct Genet 2007; 69:659–664 [View Article] [PubMed]
    [Google Scholar]
  41. McDowell MA, Johnson S, Deane JE, Cheung M, Roehrich AD et al. Structural and functional studies on the N-terminal domain of the Shigella type III secretion protein MxiG. J Biol Chem 2011; 286:30606–30614 [View Article] [PubMed]
    [Google Scholar]
  42. Bobrovskyy M, Oh SY, Missiakas D. Contribution of the EssC ATPase to the assembly of the type 7b secretion system in Staphylococcus aureus. J Biol Chem 2022; 298:102318 [View Article] [PubMed]
    [Google Scholar]
  43. Tassinari M, Doan T, Bellinzoni M, Chabalier M, Ben-Assaya M et al. The antibacterial Type VII secretion system of Bacillus subtilis: structure and interactions of the Pseudokinase YukC/EssB. mBio 2022; 13:e00134-22 [View Article] [PubMed]
    [Google Scholar]
  44. van den Ent F, Löwe J. Crystal structure of the ubiquitin-like protein YukD from Bacillus subtilis. FEBS Lett 2005; 579:3837–3841 [View Article] [PubMed]
    [Google Scholar]
  45. Klein TA, Grebenc DW, Gandhi SY, Shah VS, Kim Y et al. Structure of the extracellular region of the bacterial type VIIb secretion system subunit EsaA. Structure 2021; 29:177–185 [View Article] [PubMed]
    [Google Scholar]
  46. Dreisbach A, Hempel K, Buist G, Hecker M, Becher D et al. Profiling the surfacome of Staphylococcus aureus. PROTEOMICS 2010; 10:3082–3096 [View Article] [PubMed]
    [Google Scholar]
  47. São-José C, Baptista C, Santos MA. Bacillus subtilis operon encoding a membrane receptor for bacteriophage SPP1. J Bacteriol 2004; 186:8337–8346 [View Article] [PubMed]
    [Google Scholar]
  48. São-José C, Lhuillier S, Lurz R, Melki R, Lepault J et al. The ectodomain of the viral receptor YueB forms a fiber that triggers ejection of bacteriophage SPP1 DNA. J Biol Chem 2006; 281:11464–11470 [View Article] [PubMed]
    [Google Scholar]
  49. Zoltner M, Fyfe PK, Palmer T, Hunter WN. Characterization of Staphylococcus aureus EssB, an integral membrane component of the Type VII secretion system: atomic resolution crystal structure of the cytoplasmic segment. Biochem J 2013; 449:469–477 [View Article] [PubMed]
    [Google Scholar]
  50. Aly KA, Anderson M, Ohr RJ, Missiakas D, Silhavy TJ. Isolation of a membrane protein complex for type VII secretion in Staphylococcus aureus. J Bacteriol 2017; 199:e00482-17 [View Article] [PubMed]
    [Google Scholar]
  51. Jäger F, Zoltner M, Kneuper H, Hunter WN, Palmer T. Membrane interactions and self-association of components of the Ess/Type VII secretion system of Staphylococcus aureus. FEBS Lett 2016; 590:349–357 [View Article] [PubMed]
    [Google Scholar]
  52. Jäger F, Kneuper H, Palmer T. EssC is a specificity determinant for Staphylococcus aureus type VII secretion. Microbiology 2018; 164:816–820 [View Article] [PubMed]
    [Google Scholar]
  53. Ulhuq FR, Gomes MC, Duggan GM, Guo M, Mendonca C et al. A membrane-depolarizing toxin substrate of the Staphylococcus aureus type VII secretion system mediates intraspecies competition. Proc Natl Acad Sci U S A 2020; 117:20836–20847 [View Article] [PubMed]
    [Google Scholar]
  54. Bobrovskyy M, Willing SE, Schneewind O, Missiakas D. EssH peptidoglycan hydrolase enables Staphylococcus aureus type VII secretion across the bacterial cell wall envelope. J Bacteriol 2018; 200:e00268-18 [View Article] [PubMed]
    [Google Scholar]
  55. Kobayashi K. Diverse LXG toxin and antitoxin systems specifically mediate intraspecies competition in Bacillus subtilis biofilms. PLoS Genet 2021; 17:e1009682 [View Article] [PubMed]
    [Google Scholar]
  56. Burts ML, Williams WA, DeBord K, Missiakas DM. EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. Proc Natl Acad Sci U S A 2005; 102:1169–1174 [View Article] [PubMed]
    [Google Scholar]
  57. Korea CG, Balsamo G, Pezzicoli A, Merakou C, Tavarini S et al. Staphylococcal Esx proteins modulate apoptosis and release of intracellular Staphylococcus aureus during infection in epithelial cells. Infect Immun 2014; 82:4144–4153 [View Article] [PubMed]
    [Google Scholar]
  58. Conrad WH, Osman MM, Shanahan JK, Chu F, Takaki KK et al. Mycobacterial ESX-1 secretion system mediates host cell lysis through bacterium contact-dependent gross membrane disruptions. Proc Natl Acad Sci U S A 2017; 114:1371–1376 [View Article] [PubMed]
    [Google Scholar]
  59. Tak U, Dokland T, Niederweis M. Pore-forming Esx proteins mediate toxin secretion by Mycobacterium tuberculosis. Nat Commun 2021; 12:394 [View Article] [PubMed]
    [Google Scholar]
  60. Alhajjar N, Chatterjee A, Spencer BL, Burcham LR, Willett JLE et al. Genome-wide mutagenesis identifies factors involved in Enterococcus faecalis vaginal adherence and persistence. Infect Immun 2020; 88:e00270-20 [View Article] [PubMed]
    [Google Scholar]
  61. Bobrovskyy M, Chen X, Missiakas D. The type 7b secretion system of S. aureus and its role in colonization and systemic infection. Infect Immun 2023; 91:e00015-23 [View Article] [PubMed]
    [Google Scholar]
  62. Pinheiro J, Reis O, Vieira A, Moura IM, Zanolli Moreno L et al. Listeria monocytogenes encodes a functional ESX-1 secretion system whose expression is detrimental to in vivo infection. Virulence 2017; 8:993–1004 [View Article] [PubMed]
    [Google Scholar]
  63. Casabona MG, Buchanan G, Zoltner M, Harkins CP, Holden MTG et al. Functional analysis of the EsaB component of the Staphylococcus aureus Type VII secretion system. Microbiology 2017; 163:1851–1863 [View Article] [PubMed]
    [Google Scholar]
  64. Kobayashi K. A type VII secretion system toxin functioning as a biofilm-specific intercellular signal in Bacillus subtilis. Microbiology 2023; 2023: [View Article]
    [Google Scholar]
  65. Liu Y, Shu X, Chen L, Zhang H, Feng H et al. Plant commensal type VII secretion system causes iron leakage from roots to promote colonization. Nat Microbiol 2023; 8:1434–1449 [View Article] [PubMed]
    [Google Scholar]
  66. Zhang D, Iyer LM, Aravind L. A novel immunity system for bacterial nucleic acid degrading toxins and its recruitment in various eukaryotic and DNA viral systems. Nucleic Acids Res 2011; 39:4532–4552 [View Article] [PubMed]
    [Google Scholar]
  67. Whitney JC, Peterson SB, Kim J, Pazos M, Verster AJ et al. A broadly distributed toxin family mediates contact-dependent antagonism between gram-positive bacteria. eLife 2017; 6:e26938 [View Article] [PubMed]
    [Google Scholar]
  68. Dai Y, Wang Y, Liu Q, Gao Q, Lu H et al. A novel ESAT-6 secretion system-secreted protein EsxX of community-associated Staphylococcus aureus lineage ST398 contributes to immune evasion and virulence. Front Microbiol 2017; 8:819 [View Article] [PubMed]
    [Google Scholar]
  69. Bowran K, Garrett SR, van Vliet AHM, Palmer T. A novel variant of the Listeria monocytogenes type VII secretion system EssC component is associated with an Rhs toxin. Microb Genom 2023; 9:001036 [View Article] [PubMed]
    [Google Scholar]
  70. Cao Z, Casabona MG, Kneuper H, Chalmers JD, Palmer T. The type VII secretion system of Staphylococcus aureus secretes a nuclease toxin that targets competitor bacteria. Nat Microbiol 2016; 2:16183 [View Article] [PubMed]
    [Google Scholar]
  71. Chatterjee A, Willett JLE, Dunny GM, Duerkop BA. Phage infection and sub-lethal antibiotic exposure mediate Enterococcus faecalis type VII secretion system dependent inhibition of bystander bacteria. PLoS Genet 2021; 17:e1009204 [View Article] [PubMed]
    [Google Scholar]
  72. Klein TA, Shah PY, Gkragkopoulou P, Grebenc DW, Kim Y et al. Structure of a tripartite protein complex that targets toxins to the type VII secretion system. Microbiology 2023; 2023: [View Article]
    [Google Scholar]
  73. Garrett SR, Mietrach N, Deme J, Bitzer A, Yang Y et al. An interbacterial lipase toxin with an unprecedented reverse domain arrangement defines a new class of type VII secretion system effector. Microbiology 2023 [View Article]
    [Google Scholar]
  74. Klein TA, Pazos M, Surette MG, Vollmer W, Whitney JC. Molecular basis for immunity protein recognition of a type VII secretion system exported antibacterial toxin. J Mol Biol 2018; 430:4344–4358 [View Article] [PubMed]
    [Google Scholar]
  75. Garrett SR, Mariano G, Dicks J, Palmer T. Homologous recombination between tandem paralogues drives evolution of a subset of type VII secretion system immunity genes in firmicute bacteria. Microb Genom 2022; 8:mgen000868 [View Article] [PubMed]
    [Google Scholar]
  76. Ulhuq F. Investigating the role of TspA, a novel substrate of the Staphylococcus aureus type VII protein secretion system. n.d
  77. Liang Z, Wu H, Bian C, Chen H, Shen Y et al. The antimicrobial systems of Streptococcus suis promote niche competition in pig tonsils. Virulence 2022; 13:781–793 [View Article] [PubMed]
    [Google Scholar]
  78. Wang Y, Zhou Y, Shi C, Liu J, Lv G et al. A toxin-deformation dependent inhibition mechanism in the T7SS toxin-antitoxin system of Gram-positive bacteria. Nat Commun 2022; 13:6434 [View Article] [PubMed]
    [Google Scholar]
  79. Anderson M, Chen Y-H, Butler EK, Missiakas DM. EsaD, a secretion factor for the Ess pathway in Staphylococcus aureus. J Bacteriol 2011; 193:1583–1589 [View Article] [PubMed]
    [Google Scholar]
  80. Holberger LE, Garza-Sánchez F, Lamoureux J, Low DA, Hayes CS. A novel family of toxin/antitoxin proteins in Bacillus species. FEBS Lett 2012; 586:132–136 [View Article] [PubMed]
    [Google Scholar]
  81. Kaundal S, Deep A, Kaur G, Thakur KG. Molecular and biochemical characterization of YeeF/YezG, a polymorphic toxin-immunity protein pair from Bacillus subtilis. Front Microbiol 2020; 11:95 [View Article] [PubMed]
    [Google Scholar]
  82. Klein TA, Grebenc DW, Shah PY, McArthur OD, Dickson BH et al. Dual targeting factors are required for LXG toxin export by the bacterial type VIIb secretion system. mBio 2022; 13:e02137-22 [View Article] [PubMed]
    [Google Scholar]
  83. Ruhe ZC, Low DA, Hayes CS. Polymorphic toxins and their immunity proteins: diversity, evolution, and mechanisms of delivery. Annu Rev Microbiol 2020; 74:497–520 [View Article] [PubMed]
    [Google Scholar]
  84. Virtanen P, Wäneskog M, Koskiniemi S. Class II contact-dependent growth inhibition (CDI) systems allow for broad-range cross-species toxin delivery within the Enterobacteriaceae family. Mol Microbiol 2019; 111:1109–1125 [View Article] [PubMed]
    [Google Scholar]
  85. Coulthurst S. The Type VI secretion system: a versatile bacterial weapon. Microbiology 2019; 165:503–515 [View Article] [PubMed]
    [Google Scholar]
  86. Klein TA, Ahmad S, Whitney JC. Contact-dependent interbacterial antagonism mediated by protein secretion machines. Trends Microbiol 2020; 28:387–400 [View Article] [PubMed]
    [Google Scholar]
  87. Baptista C, Barreto HC, São-José C. High levels of DegU-P activate an Esat-6-like secretion system in Bacillus subtilis. PLoS One 2013; 8:e67840 [View Article] [PubMed]
    [Google Scholar]
  88. Krismer B, Liebeke M, Janek D, Nega M, Rautenberg M et al. Nutrient limitation governs Staphylococcus aureus metabolism and niche adaptation in the human nose. PLoS Pathog 2014; 10:e1003862 [View Article] [PubMed]
    [Google Scholar]
  89. Deng L, Schilcher K, Burcham LR, Kwiecinski JM, Johnson PM et al. Identification of key determinants of Staphylococcus aureus vaginal colonization. mBio 2019; 10:e02321-19 [View Article] [PubMed]
    [Google Scholar]
  90. Bischoff M, Entenza JM, Giachino P. Influence of a functional sigB operon on the global regulators sar and agr in Staphylococcus aureus. J Bacteriol 2001; 183:5171–5179 [View Article] [PubMed]
    [Google Scholar]
  91. Dunman PM, Murphy E, Haney S, Palacios D, Tucker-Kellogg G et al. Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J Bacteriol 2001; 183:7341–7353 [View Article] [PubMed]
    [Google Scholar]
  92. Schulthess B, Bloes DA, Berger-Bächi B. Opposing roles of σB and σB-controlled SpoVG in the global regulation of esxA in Staphylococcus aureus. BMC Microbiol 2012; 12:17 [View Article] [PubMed]
    [Google Scholar]
  93. Crosby HA, Tiwari N, Kwiecinski JM, Xu Z, Dykstra A et al. The Staphylococcus aureus ArlRS two-component system regulates virulence factor expression through MgrA. Mol Microbiol 2020; 113:103–122 [View Article] [PubMed]
    [Google Scholar]
  94. Anderson M, Aly KA, Chen Y-H, Missiakas D. Secretion of atypical protein substrates by the ESAT-6 secretion system of Staphylococcus aureus. Mol Microbiol 2013; 90:734–743 [View Article] [PubMed]
    [Google Scholar]
  95. Jenul C, Horswill AR. Regulation of Staphylococcus aureus virulence. Microbiol Spectr 2019; 7:7
    [Google Scholar]
  96. Karlsson-Kanth A, Tegmark-Wisell K, Arvidson S, Oscarsson J. Natural human isolates of Staphylococcus aureus selected for high production of proteases and alpha-hemolysin are sigmaB deficient. Int J Med Microbiol 2006; 296:229–236 [View Article] [PubMed]
    [Google Scholar]
  97. Shopsin B, Drlica-Wagner A, Mathema B, Adhikari RP, Kreiswirth BN et al. Prevalence of agr dysfunction among colonizing Staphylococcus aureus strains. J Infect Dis 2008; 198:1171–1174 [View Article] [PubMed]
    [Google Scholar]
  98. Yang Y, Alcock F, Kneuper H, Palmer T. A high throughput assay to measure Type VII secretion in Staphylococcus aureus. Microbiology 2023 [View Article]
    [Google Scholar]
  99. Lopez MS, Tan IS, Yan D, Kang J, McCreary M et al. Host-derived fatty acids activate type VII secretion in Staphylococcus aureus. Proc Natl Acad Sci U S A 2017; 114:11223–11228 [View Article] [PubMed]
    [Google Scholar]
  100. Mielich-Süss B, Wagner RM, Mietrach N, Hertlein T, Marincola G et al. Flotillin scaffold activity contributes to type VII secretion system assembly in Staphylococcus aureus. PLoS Pathog 2017; 13:e1006728 [View Article] [PubMed]
    [Google Scholar]
  101. Casabona MG, Kneuper H, Alferes de Lima D, Harkins CP, Zoltner M et al. Haem-iron plays a key role in the regulation of the Ess/type VII secretion system of Staphylococcus aureus RN6390. Microbiology 2017; 163:1839–1850 [View Article] [PubMed]
    [Google Scholar]
  102. Kobayashi K. Gradual activation of the response regulator DegU controls serial expression of genes for flagellum formation and biofilm formation in Bacillus subtilis. Mol Microbiol 2007; 66:395–409 [View Article] [PubMed]
    [Google Scholar]
  103. Basler M, Ho BT, Mekalanos JJ. Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 2013; 152:884–894 [View Article] [PubMed]
    [Google Scholar]
  104. Gonzalez D, Mavridou DAI. Making the best of aggression: the many dimensions of bacterial toxin regulation. Trends Microbiol 2019; 27:897–905 [View Article] [PubMed]
    [Google Scholar]
  105. Kamal F, Liang X, Manera K, Pei T-T, Kim H et al. Differential cellular response to translocated toxic effectors and physical penetration by the Type VI secretion system. Cell Rep 2020; 31:107766 [View Article] [PubMed]
    [Google Scholar]
  106. Manuse S, Fleurie A, Zucchini L, Lesterlin C, Grangeasse C. Role of eukaryotic-like serine/threonine kinases in bacterial cell division and morphogenesis. FEMS Microbiol Rev 2016; 40:41–56 [View Article] [PubMed]
    [Google Scholar]
  107. Pensinger DA, Schaenzer AJ, Sauer J-D. Do shoot the messenger: PASTA kinases as virulence determinants and antibiotic targets. Trends Microbiol 2018; 26:56–69 [View Article] [PubMed]
    [Google Scholar]
  108. Alcock F, Palmer T. Activation of a bacterial killing machine. PLoS Genet 2021; 17:e1009261 [View Article] [PubMed]
    [Google Scholar]
  109. Yang Y, Boardman E, Deme J, Alcock F, Lea S et al. Three small partner proteins facilitate the type VII-dependent secretion of an antibacterial nuclease. mBio 2023; 14:e02100-23 [View Article] [PubMed]
    [Google Scholar]
  110. Daleke MH, Ummels R, Bawono P, Heringa J, Vandenbroucke-Grauls CMJE et al. General secretion signal for the mycobacterial type VII secretion pathway. Proc Natl Acad Sci U S A 2012; 109:11342–11347 [View Article] [PubMed]
    [Google Scholar]
  111. Solomonson M, Setiaputra D, Makepeace KAT, Lameignere E, Petrotchenko EV et al. Structure of EspB from the ESX-1 type VII secretion system and insights into its export mechanism. Structure 2015; 23:571–583 [View Article] [PubMed]
    [Google Scholar]
  112. Strong M, Sawaya MR, Wang S, Phillips M, Cascio D et al. Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 2006; 103:8060–8065 [View Article] [PubMed]
    [Google Scholar]
  113. Ekiert DC, Cox JS. Structure of a PE-PPE-EspG complex from Mycobacterium tuberculosis reveals molecular specificity of ESX protein secretion. Proc Natl Acad Sci U S A 2014; 111:14758–14763 [View Article] [PubMed]
    [Google Scholar]
  114. Korotkova N, Piton J, Wagner JM, Boy-Röttger S, Japaridze A et al. Structure of EspB, a secreted substrate of the ESX-1 secretion system of Mycobacterium tuberculosis. J Struct Biol 2015; 191:236–244 [View Article] [PubMed]
    [Google Scholar]
  115. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998; 393:537–544 [View Article] [PubMed]
    [Google Scholar]
  116. Williamson ZA, Chaton CT, Ciocca WA, Korotkova N, Korotkov KV. PE5-PPE4-EspG3 heterotrimer structure from mycobacterial ESX-3 secretion system gives insight into cognate substrate recognition by ESX systems. J Biol Chem 2020; 295:12706–12715 [View Article] [PubMed]
    [Google Scholar]
  117. Phan TH, Ummels R, Bitter W, Houben ENG. Identification of a substrate domain that determines system specificity in mycobacterial type VII secretion systems. Sci Rep 2017; 7:42704 [View Article] [PubMed]
    [Google Scholar]
  118. Chen X, Cheng H-F, Zhou J, Chan C-Y, Lau K-F et al. Structural basis of the PE-PPE protein interaction in Mycobacterium tuberculosis. J Biol Chem 2017; 292:16880–16890 [View Article] [PubMed]
    [Google Scholar]
  119. Gijsbers A, Eymery M, Gao Y, Menart I, Vinciauskaite V et al. The crystal structure of the EspB-EspK virulence factor-chaperone complex suggests an additional type VII secretion mechanism in Mycobacterium tuberculosis. J Biol Chem 2023; 299:102761 [View Article] [PubMed]
    [Google Scholar]
  120. Ahmed MM, Aboshanab KM, Ragab YM, Missiakas DM, Aly KA. The transmembrane domain of the Staphylococcus aureus ESAT-6 component EssB mediates interaction with the integral membrane protein EsaA, facilitating partially regulated secretion in a heterologous host. Arch Microbiol 2018; 200:1075–1086 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001420
Loading
/content/journal/micro/10.1099/mic.0.001420
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error