Signal peptides direct surface proteins to two distinct envelope locations of Staphylococcus aureus.
Surface proteins of Gram-positive bacteria are covalently linked to the cell wall envelope by a mechanism requiring an N-terminal signal peptide and a C-terminal LPXTG motif sorting signal. We show here that surface proteins of Staphylococcus aureus arrive at two distinct destinations in the bacterial envelope, either distributed as a ring surrounding each cell or as discrete assembly sites. Proteins with ring-like distribution (clumping factor A (ClfA), Spa, fibronectin-binding protein B (FnbpB), serine-aspartate repeat protein C (SdrC) and SdrD) harbour signal peptides with a YSIRK/GS motif, whereas proteins directed to discrete assembly sites (S. aureus surface protein A (SasA), SasD, SasF and SasK) do not. Reciprocal exchange of signal peptides between surface proteins with (ClfA) or without the YSIRK/GS motif (SasF) directed recombinant products to the alternate destination, whereas mutations that altered only the YSIRK sequence had no effect. Our observations suggest that S. aureus distinguishes between signal peptides to address proteins to either the cell pole (signal peptides without YSIRK/GS) or the cross wall, the peptidoglycan layer that forms during cell division to separate new daughter cells (signal peptides with YISRK/GS motif).
DeDent
Andrea
A
Department of Microbiology, University of Chicago, Chicago, IL 60637, USA.
Bae
Taeok
T
Missiakas
Dominique M
DM
Schneewind
Olaf
O
D020816:Amino Acid Motifs; D000595:Amino Acid Sequence; D003030:Coagulase / Q000737:chemistry; D008565:Membrane Proteins / Q000378:metabolism; D018613:Microscopy, Confocal; D008954:Models, Biological; D008969:Molecular Sequence Data; D010455:Peptides / Q000737:chemistry; D021382:Protein Sorting Signals / Q000235:genetics*; D017434:Protein Structure, Tertiary; D011994:Recombinant Proteins / Q000737:chemistry; D017386:Sequence Homology, Amino Acid; D013211:Staphylococcus aureus / Q000378:metabolism*; D013499:Surface Properties; D014357:Trypsin / Q000737:chemistry
C515944:ClfA protein, Staphylococcus aureus; D003030:Coagulase; D008565:Membrane Proteins; D010455:Peptides; D021382:Protein Sorting Signals; D011994:Recombinant Proteins; D014357:Trypsin
Nature. 1983 Oct 20-26;305(5936):709-12
6226876
Microbiol Mol Biol Rev. 1999 Mar;63(1):174-229
10066836
Science. 1995 Apr 7;268(5207):103-6
7701329
Gene. 1991 Jul 15;103(1):101-5
1652539
Nature. 1959 Jul 25;184:247-8
13794315
Mol Microbiol. 2001 Jun;40(5):1049-57
11401711
Cell. 1992 Jul 24;70(2):267-81
1638631
Proc Natl Acad Sci U S A. 1965 Aug;54(2):587-94
5218655
Biochimie. 2000 Nov;82(11):1005-14
11099797
APMIS. 2007 May;115(5):533-9; discussion 540-1
17504410
Mol Microbiol. 2002 May;44(4):1081-94
12010500
J Biol Chem. 2002 May 3;277(18):16241-8
11856734
Proc Natl Acad Sci U S A. 2006 Nov 7;103(45):16942-7
17075065
Mol Microbiol. 2003 Jun;48(6):1429-49
12791129
Science. 1993 Jul 16;261(5119):308-9
8392747
J Bacteriol. 1969 Jan;97(1):396-401
5764340
J Biol Chem. 1998 Oct 30;273(44):29135-42
9786922
J Cell Biol. 1970 Dec;47(3):786-90
4395735
Biochemistry. 1967 Dec;6(12):3659-70
4864856
Nature. 1991 Nov 14;354(6349):161-4
1944597
Proc Natl Acad Sci U S A. 2004 Aug 17;101(33):12312-7
15304642
Science. 2001 Jul 20;293(5529):498-506
11463916
Science. 1999 Jul 30;285(5428):760-3
10427003
J Mol Biol. 1992 May 20;225(2):487-94
1593632
J Bacteriol. 2003 May;185(9):2910-9
12700270
Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):285-9
7816834
J Bacteriol. 2004 Nov;186(21):7100-11
15489421
Proc Natl Acad Sci U S A. 1967 Jun;57(6):1878-84
5231417
J Biol Chem. 2000 Mar 31;275(13):9876-81
10734144
J Biol Chem. 1998 Oct 30;273(44):29143-9
9786923
Int Rev Cytol. 1976;44:225-318
770370
J Biol Chem. 1999 Aug 20;274(34):24316-20
10446208
J Bacteriol. 1969 Oct;100(1):505-11
4899006
Science. 1962 Mar 2;135(3505):722-4
13880442
Adv Microb Physiol. 2003;47:187-254
14560665
J Bacteriol. 2007 Jun;189(12):4473-84
17416657
Annu Rev Genet. 1990;24:249-74
2088169
J Bacteriol. 1977 Jan;129(1):343-50
830642
Microbiol Mol Biol Rev. 1998 Dec;62(4):1371-414
9841676
J Bacteriol. 2007 May;189(10):3846-54
17369296
Microbiol Mol Biol Rev. 2006 Mar;70(1):192-221
16524923
Proc Natl Acad Sci U S A. 1978 Dec;75(12):5802-6
104291
J Bacteriol. 2004 Jun;186(11):3286-95
15150213
J Bacteriol. 2007 Mar;189(6):2521-30
17209021
EMBO J. 1998 Aug 17;17(16):4639-46
9707423
J Mol Biol. 1983 Jun 5;166(4):557-80
6345791
Mol Microbiol. 2003 Nov;50(3):871-81
14617148
J Biol Chem. 1962 Dec;237:3603-13
13976222
Harvey Lect. 1968-1969;64:179-213
4926386
Nature. 1952 Nov 1;170(4331):746-7
13002428
Nature. 2006 Aug 24;442(7105):943-6
16929299
J Gen Microbiol. 1952 Feb;6(1-2):95-107
14927856
J Exp Med. 1928 Jan 1;47(1):91-103
19869404
J Bacteriol. 1996 Mar;178(6):1565-71
8626282
EMBO J. 1993 Dec;12(12):4803-11
8223489
Mol Microbiol. 1994 Oct;14(1):115-21
7830549
J Exp Med. 1963 Nov 1;118:659-66
14087613
J Bacteriol. 2008 Jan;190(1):300-10
17951380
Mol Microbiol. 1993 Aug;9(3):403-9
8412689
Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6172-6
1385871