title: Synthetic effects of secG and secY2 mutations on exoproteome biogenesis in Staphylococcus aureus.
abstract: The gram-positive pathogen Staphylococcus aureus secretes various proteins into its extracellular milieu. Bioinformatics analyses have indicated that most of these proteins are directed to the canonical Sec pathway, which consists of the translocation motor SecA and a membrane-embedded channel composed of the SecY, SecE, and SecG proteins. In addition, S. aureus contains an accessory Sec2 pathway involving the SecA2 and SecY2 proteins. Here, we have addressed the roles of the nonessential channel components SecG and SecY2 in the biogenesis of the extracellular proteome of S. aureus. The results show that SecG is of major importance for protein secretion by S. aureus. Specifically, the extracellular accumulation of nine abundant exoproteins and seven cell wall-bound proteins was significantly affected in an secG mutant. No secretion defects were detected for strains with a secY2 single mutation. However, deletion of secY2 exacerbated the secretion defects of secG mutants, affecting the extracellular accumulation of one additional exoprotein and one cell wall protein. Furthermore, an secG secY2 double mutant displayed a synthetic growth defect. This might relate to a slightly elevated expression of sraP, encoding the only known substrate for the Sec2 pathway, in cells lacking SecG. Additionally, the results suggest that SecY2 can interact with the Sec1 channel, which would be consistent with the presence of a single set of secE and secG genes in S. aureus.
authors.affiliation: Department of Medical Microbiology, University Medical Center Groningen and University of Groningen, Hanzeplein 1, P.O. Box 30001, 9700 RB Groningen, The Netherlands.
authors.forename: Mark J J B
authors.initials: MJ
authors.lastname: Sibbald
authors.forename: Theresa
authors.initials: T
authors.lastname: Winter
authors.forename: Magdalena M
authors.initials: MM
authors.lastname: van der Kooi-Pol
authors.forename: G
authors.initials: G
authors.lastname: Buist
authors.forename: E
authors.initials: E
authors.lastname: Tsompanidou
authors.forename: Tjibbe
authors.initials: T
authors.lastname: Bosma
authors.forename: Tina
authors.initials: T
authors.lastname: Schäfer
authors.forename: Knut
authors.initials: K
authors.lastname: Ohlsen
authors.forename: Michael
authors.initials: M
authors.lastname: Hecker
authors.forename: Haike
authors.initials: H
authors.lastname: Antelmann
authors.forename: Susanne
authors.initials: S
authors.lastname: Engelmann
authors.forename: Jan Maarten
authors.initials: JM
authors.lastname: van Dijl
mesh_terms: D000818:Animals; D001426:Bacterial Proteins / Q000235:genetics* / Q000378:metabolism*; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial / Q000502:physiology*; D051379:Mice; D009154:Mutation; D013203:Staphylococcal Infections / Q000382:microbiology; D013211:Staphylococcus aureus / Q000235:genetics / Q000378:metabolism* / Q000472:pathogenicity; D014158:Transcription, Genetic; D014774:Virulence
chemical_list: D001426:Bacterial Proteins
references.citation: Mol Microbiol. 2002 May;44(4):1081-94
references.pmid: 12010500
references.citation: Mol Immunol. 2008 Mar;45(6):1600-11
references.pmid: 18061675
references.citation: Annu Rev Biochem. 2008;77:643-67
references.pmid: 18078384
references.citation: Science. 2003 Nov 28;302(5650):1569-71
references.pmid: 14645850
references.citation: Nature. 2008 Oct 16;455(7215):936-43
references.pmid: 18923516
references.citation: Cell. 1992 Jul 24;70(2):267-81
references.pmid: 1638631
references.citation: Cell. 1997 Nov 28;91(5):563-6
references.pmid: 9393849
references.citation: Electrophoresis. 1999 Aug;20(11):2225-40
references.pmid: 10493127
references.citation: J Bacteriol. 2006 Feb;188(3):1188-90
references.pmid: 16428426
references.citation: Infect Immun. 2005 Apr;73(4):2273-80
references.pmid: 15784571
references.citation: J Antimicrob Chemother. 1997 Jul;40(1):135-6
references.pmid: 9249217
references.citation: Biochim Biophys Acta. 2004 Nov 11;1694(1-3):279-97
references.pmid: 15546672
references.citation: Cell. 1988 Nov 18;55(4):683-92
references.pmid: 2846186
references.citation: EMBO J. 1993 Sep;12(9):3409-15
references.pmid: 8253068
references.citation: J Bacteriol. 2006 Nov;188(22):7742-58
references.pmid: 17079681
references.citation: Nature. 1983 Oct 20-26;305(5936):709-12
references.pmid: 6226876
references.citation: Mol Microbiol. 2008 May;68(4):838-47
references.pmid: 18430080
references.citation: Infect Immun. 1987 Dec;55(12):3103-10
references.pmid: 3679545
references.citation: J Biol Chem. 2008 Jun 20;283(25):17579-93
references.pmid: 18434316
references.citation: Appl Environ Microbiol. 2004 Oct;70(10):6076-85
references.pmid: 15466553
references.citation: J Biol Chem. 2007 Oct 5;282(40):29540-8
references.pmid: 17704542
references.citation: FEBS J. 2005 Sep;272(18):4617-30
references.pmid: 16156784
references.citation: Appl Environ Microbiol. 2004 Nov;70(11):6887-91
references.pmid: 15528558
references.citation: Mol Gen Genet. 1999 Apr;261(3):558-66
references.pmid: 10323238
references.citation: J Bacteriol. 1999 Mar;181(6):1786-92
references.pmid: 10074070
references.citation: Methods Enzymol. 1991;204:587-636
references.pmid: 1658572
references.citation: Proteomics. 2004 Oct;4(10):3034-47
references.pmid: 15378746
references.citation: Antimicrob Agents Chemother. 2009 Nov;53(11):4702-11
references.pmid: 19738010
references.citation: Gene. 1995 Dec 29;167(1-2):335-6
references.pmid: 8566804
references.citation: Electrophoresis. 2004 May;25(9):1327-33
references.pmid: 15174055
references.citation: Trends Microbiol. 2001 Dec;9(12):605-10
references.pmid: 11728874
references.citation: J Bacteriol. 2007 Oct;189(20):7316-25
references.pmid: 17675373
references.citation: Cell. 1996 Apr 5;85(1):71-81
references.pmid: 8620539
references.citation: J Chromatogr B Analyt Technol Biomed Life Sci. 2007 Apr 15;849(1-2):129-40
references.pmid: 17055787
references.citation: Microbiol Mol Biol Rev. 2000 Sep;64(3):515-47
references.pmid: 10974125
references.citation: Microbiology (Reading). 1999 Feb;145 ( Pt 2):357-366
references.pmid: 10075418
references.citation: Gene. 1983 Dec;26(1):101-6
references.pmid: 6323249
references.citation: J Biochem. 2000 Jul;128(1):129-37
references.pmid: 10876167
references.citation: J Mol Biol. 1983 Jun 5;166(4):557-80
references.pmid: 6345791
references.citation: Microbiol Mol Biol Rev. 2006 Sep;70(3):755-88
references.pmid: 16959968
references.citation: J Immunol. 1991 Sep 15;147(6):1877-83
references.pmid: 1909733
references.citation: J Bacteriol. 2005 Jun;187(11):3878-83
references.pmid: 15901716
references.citation: Microbiology (Reading). 1998 Apr;144 ( Pt 4):985-991
references.pmid: 9579072
references.citation: Cell Mol Life Sci. 2010 Jan;67(2):179-99
references.pmid: 19823765
references.citation: Microbiology (Reading). 1999 Apr;145 ( Pt 4):801-808
references.pmid: 10220159
references.citation: Genome Res. 2001 Sep;11(9):1484-502
references.pmid: 11544192
references.citation: Nat Rev Microbiol. 2007 Nov;5(11):839-51
references.pmid: 17938627
references.citation: Proteomics. 2006 Jun;6(12):3636-48
references.pmid: 16705751
references.citation: J Bacteriol. 2008 Sep;190(18):6188-96
references.pmid: 18621893
references.citation: Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4678-83
references.pmid: 12682299
references.citation: J Bacteriol. 1992 May;174(10):3300-10
references.pmid: 1339421
references.citation: Proteomics. 2010 Apr;10(8):1634-44
references.pmid: 20186749
references.citation: Proc Natl Acad Sci U S A. 2005 Nov 29;102(48):17466-71
references.pmid: 16293689
references.citation: Cell. 1990 Aug 24;62(4):649-57
references.pmid: 2167176
references.citation: FEBS Lett. 1996 Feb 26;381(1-2):25-8
references.pmid: 8641431
references.citation: Proteomics. 2004 Oct;4(10):2849-76
references.pmid: 15378759
references.citation: J Bacteriol. 2002 Oct;184(19):5457-67
references.pmid: 12218034