Home LiteratureArticle Details
PMID: 20847047 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Staphylococcal major autolysin (Atl) is involved in excretion of cytoplasmic proteins.

The Journal of biological chemistry ·Vol. 285 ·No. 47 ·2010-11-19 ·Pages 36794-803

Pasztor L, Ziebandt AK, Nega M, Schlag M, Haase S, Franz-Wachtel M, Madlung J, Nordheim A, Heinrichs DE, Götz F

Abstract

Many microorganisms excrete typical cytoplasmic proteins into the culture supernatant. As none of the classical secretion systems appears to be involved, this type of secretion was referred to as "nonclassical protein secretion." Here, we demonstrate that in Staphylococcus aureus the major autolysin plays a crucial role in release of cytoplasmic proteins. Comparative secretome analysis revealed that in the wild type S. aureus strain, 22 typical cytoplasmic proteins were excreted into the culture supernatant, although in the atl mutant they were significantly decreased. The presence or absence of prophages had little influence on the secretome pattern. In the atl mutant, secondary peptidoglycan hydrolases were increased in the secretome; the corresponding genes were transcriptionally up-regulated suggesting a compensatory mechanism for the atl mutation. Using glyceraldehyde-3-phosphate dehydrogenase (GAPDH) as a cytoplasmic indicator enzyme, we showed that all clinical isolates tested excreted this protein. In the wall teichoic acid-deficient tagO mutant with its increased autolysis activity, GAPDH was excreted in even higher amounts than in the WT, confirming the importance of autolysis in excretion of cytoplasmic proteins. To answer the question of how discriminatory the excretion of cytoplasmic proteins is, we performed a two-dimensional PAGE of cytoplasmic proteins isolated from WT. Surprisingly, the most abundant proteins in the cytoplasm were not found in the secretome of the WT, suggesting that there exists a selection mechanism in the excretion of cytoplasmic proteins. As the major autolysin binds at the septum site, we assume that the proteins are preferentially released at and during septum formation.

MeSH Terms
Bacterial Proteins/metabolism Blotting, Northern Blotting, Western Cytoplasm/metabolism Electrophoresis, Gel, Two-Dimensional Humans Image Processing, Computer-Assisted N-Acetylmuramoyl-L-alanine Amidase/genetics,metabolism RNA, Messenger/genetics Reverse Transcriptase Polymerase Chain Reaction Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization Staphylococcal Infections/metabolism Staphylococcus aureus/pathogenicity
Chemicals
Bacterial Proteins RNA, Messenger N-Acetylmuramoyl-L-alanine Amidase
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Pasztor Linda
Department of Microbial Genetics, University of Tübingen, D-72076 Tübingen, Germany.
Ziebandt Anne-Kathrin
Nega Mulugeta
Schlag Martin
Haase Sabine
Franz-Wachtel Mirita
Madlung Johannes
Nordheim Alfred
Heinrichs David E
Götz Friedrich
References (59)
59 references, click to expand
  1. Extracellular proteins of Staphylococcus aureus and the role of SarA and sigma B.
    Proteomics. 2001 Apr;1(4):480-93 PMID: 11681202
  2. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  3. Characterization of toxin production of coagulase-negative staphylococci isolated from food and starter cultures.
    Int J Food Microbiol. 2008 Oct 31;127(3):246-51 PMID: 18752861
  4. Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates.
    Infect Immun. 2010 Jun;78(6):2877-89 PMID: 20212089
  5. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus.
    Virology. 1967 Sep;33(1):155-66 PMID: 4227577
  6. Whole genome sequencing of meticillin-resistant Staphylococcus aureus.
    Lancet. 2001 Apr 21;357(9264):1225-40 PMID: 11418146
  7. Biogenesis of bacterial membrane vesicles.
    Mol Microbiol. 2009 Jun;72(6):1395-407 PMID: 19432795
  8. Is 2-phosphoglycerate-dependent automodification of bacterial enolases implicated in their export?
    J Mol Biol. 2004 Mar 19;337(2):485-96 PMID: 15003462
  9. Simultaneous and rapid isolation of bacterial and eukaryotic DNA and RNA: a new approach for isolating DNA.
    Biotechniques. 1991 Jul;11(1):94-101 PMID: 1720004
  10. Two restriction and modification systems in Staphylococcus aureus NCTC8325.
    J Gen Microbiol. 1976 Oct;96(2):277-81 PMID: 136497
  11. Holins: form and function in bacteriophage lysis.
    FEMS Microbiol Rev. 1995 Aug;17(1-2):191-205 PMID: 7669346
  12. Penicillinase production and intrinsic resistance to penicillins in Staphylococcus aures.
    Lancet. 1966 Apr 16;1(7442):835-8 PMID: 4159958
  13. Staphylococcus aureus ClpC ATPase is a late growth phase effector of metabolism and persistence.
    Proteomics. 2009 Mar;9(5):1152-76 PMID: 19253280
  14. Proteomics of protein secretion by Bacillus subtilis: separating the "secrets" of the secretome.
    Microbiol Mol Biol Rev. 2004 Jun;68(2):207-33 PMID: 15187182
  15. ABC transporters of staphylococci.
    Res Microbiol. 2001 Apr-May;152(3-4):351-6 PMID: 11421282
  16. Comparative proteome analysis of secretory proteins from pathogenic and nonpathogenic Listeria species.
    Proteomics. 2005 Apr;5(6):1544-57 PMID: 15838904
  17. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling.
    Proteomics. 2006 Mar;6(6):1867-77 PMID: 16470655
  18. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis.
    Mol Microbiol. 1996 Jun;20(5):1083-91 PMID: 8809760
  19. A proteomic view of an important human pathogen--towards the quantification of the entire Staphylococcus aureus proteome.
    PLoS One. 2009 Dec 04;4(12):e8176 PMID: 19997597
  20. A Staphylococcus aureus autolysin that has an N-acetylmuramoyl-L-alanine amidase domain and an endo-beta-N-acetylglucosaminidase domain: cloning, sequence analysis, and characterization.
    Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):285-9 PMID: 7816834
  21. Regulation of sigmaB-dependent transcription of sigB and asp23 in two different Staphylococcus aureus strains.
    Mol Gen Genet. 1999 Apr;261(3):558-66 PMID: 10323238
  22. An exocyst complex functions in plant cell growth in Arabidopsis and tobacco.
    Plant Cell. 2008 May;20(5):1330-45 PMID: 18492870
  23. The influence of agr and sigmaB in growth phase dependent regulation of virulence factors in Staphylococcus aureus.
    Proteomics. 2004 Oct;4(10):3034-47 PMID: 15378746
  24. Role of the twin-arginine translocation pathway in Staphylococcus.
    J Bacteriol. 2009 Oct;191(19):5921-9 PMID: 19633084
  25. Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database.
    J Clin Microbiol. 2003 Nov;41(11):5113-20 PMID: 14605147
  26. Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model.
    J Infect Dis. 2001 Apr 1;183(7):1038-42 PMID: 11237828
  27. Producer self-protection against the lantibiotic epidermin by the ABC transporter EpiFEG of Staphylococcus epidermidis Tü3298.
    FEMS Microbiol Lett. 1998 Sep 15;166(2):203-11 PMID: 9770275
  28. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis.
    Electrophoresis. 2004 May;25(9):1327-33 PMID: 15174055
  29. Proteomics in gram-negative bacterial outer membrane vesicles.
    Mass Spectrom Rev. 2008 Nov-Dec;27(6):535-55 PMID: 18421767
  30. Variation in the antigenic composition of staphylococcal coagulase.
    J Gen Microbiol. 1952 Nov;7(3-4):320-6 PMID: 13022917
  31. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles.
    Proteomics. 2009 Dec;9(24):5425-36 PMID: 19834908
  32. Proteome analyses of Staphylococcus aureus in growing and non-growing cells: a physiological approach.
    Int J Med Microbiol. 2005 Dec;295(8):547-65 PMID: 16325551
  33. Comparative proteomic analysis of extracellular proteins of enterohemorrhagic and enteropathogenic Escherichia coli strains and their ihf and ler mutants.
    Appl Environ Microbiol. 2004 Sep;70(9):5274-82 PMID: 15345410
  34. Mapping the pathways to staphylococcal pathogenesis by comparative secretomics.
    Microbiol Mol Biol Rev. 2006 Sep;70(3):755-88 PMID: 16959968
  35. Activity of the major staphylococcal autolysin Atl.
    FEMS Microbiol Lett. 2006 Jun;259(2):260-8 PMID: 16734789
  36. Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation.
    Infect Immun. 1996 Jan;64(1):277-82 PMID: 8557351
  37. Genome engineering reveals large dispensable regions in Bacillus subtilis.
    Mol Biol Evol. 2003 Dec;20(12):2076-90 PMID: 12949151
  38. Synthetic effects of secG and secY2 mutations on exoproteome biogenesis in Staphylococcus aureus.
    J Bacteriol. 2010 Jul;192(14):3788-800 PMID: 20472795
  39. Structure-function analysis of PrsA reveals roles for the parvulin-like and flanking N- and C-terminal domains in protein folding and secretion in Bacillus subtilis.
    J Biol Chem. 2004 Apr 30;279(18):19302-14 PMID: 14976191
  40. Comparison of the extracellular proteomes of Escherichia coli B and K-12 strains during high cell density cultivation.
    Proteomics. 2008 May;8(10):2089-103 PMID: 18425732
  41. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule.
    EMBO J. 1993 Oct;12(10):3967-75 PMID: 7691599
  42. A comprehensive two-dimensional map of cytosolic proteins of Bacillus subtilis.
    Electrophoresis. 2001 Aug;22(14):2908-35 PMID: 11565787
  43. Non-classical protein secretion in bacteria.
    BMC Microbiol. 2005 Oct 07;5:58 PMID: 16212653
  44. A defect in menadione biosynthesis induces global changes in gene expression in Staphylococcus aureus.
    J Bacteriol. 2008 Oct;190(19):6351-64 PMID: 18676673
  45. Anaerobic gene expression in Staphylococcus aureus.
    J Bacteriol. 2007 Jun;189(11):4275-89 PMID: 17384184
  46. Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis.
    Infect Immun. 1995 Sep;63(9):3373-80 PMID: 7642265
  47. Phage release from biofilm and planktonic Staphylococcus aureus cells.
    FEMS Microbiol Lett. 2005 Nov 1;252(1):89-96 PMID: 16213676
  48. Comparative analysis of the genomes of the temperate bacteriophages phi 11, phi 12 and phi 13 of Staphylococcus aureus 8325.
    Gene. 2002 May 1;289(1-2):109-18 PMID: 12036589
  49. Leaky Lactococcus cultures that externalize enzymes and antigens independently of culture lysis and secretion and export pathways.
    Appl Environ Microbiol. 2001 Jan;67(1):251-9 PMID: 11133453
  50. Role of staphylococcal wall teichoic acid in targeting the major autolysin Atl.
    Mol Microbiol. 2010 Feb;75(4):864-73 PMID: 20105277
  51. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections.
    Nat Med. 2004 Mar;10(3):243-5 PMID: 14758355
  52. An autolysin ring associated with cell separation of Staphylococcus aureus.
    J Bacteriol. 1996 Mar;178(6):1565-71 PMID: 8626282
  53. Structural basis of cell wall cleavage by a staphylococcal autolysin.
    PLoS Pathog. 2010 Mar 12;6(3):e1000807 PMID: 20300605
  54. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface.
    Mol Microbiol. 1997 Jun;24(5):1013-24 PMID: 9220008
  55. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa.
    Anal Biochem. 1987 Nov 1;166(2):368-79 PMID: 2449095
  56. A comprehensive proteome map of growing Bacillus subtilis cells.
    Proteomics. 2004 Oct;4(10):2849-76 PMID: 15378759
  57. EsaC substrate for the ESAT-6 secretion pathway and its role in persistent infections of Staphylococcus aureus.
    Mol Microbiol. 2008 Aug;69(3):736-46 PMID: 18554323
  58. Transferrin binding in Staphylococcus aureus: involvement of a cell wall-anchored protein.
    Mol Microbiol. 2002 Mar;43(6):1603-14 PMID: 11952908
  59. The elastin-binding protein of Staphylococcus aureus (EbpS) is expressed at the cell surface as an integral membrane protein and not as a cell wall-associated protein.
    J Biol Chem. 2002 Jan 4;277(1):243-50 PMID: 11684686
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2010-11-19
Epub
2010-00-16
Pages
36794-803
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2978608
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com