Previous Article | Next Article 
Journal of Bacteriology, April 2002, p. 2181-2191, Vol. 184, No. 8
0021-9193/02/$04.00+0 DOI: 10.1128/JB.184.8.2181-2191.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.
Differential Recognition of Surface Proteins in Streptococcus pyogenes by Two Sortase Gene Homologs
Timothy C. Barnett and June R. Scott*
Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, Georgia 30322
Received 28 November 2001/
Accepted 17 January 2002
The interaction of Streptococcus pyogenes (group A streptococcus [GAS]) with its human host requires several surface proteins. In this study, we isolated mutations in a gene required for the surface localization of protein F by transposon mutagenesis of the M6 strain JRS4. This gene (srtA) encodes a protein homologous to Staphylococcus aureus sortase, which covalently links proteins containing an LPXTG motif to the cell wall. The GAS srtA mutant was defective in anchoring the LPXTG-containing proteins M6, protein F, ScpA, and GRAB to the cell surface. This phenotype was complemented when a wild-type srtA gene was provided in trans. The surface localization of T6, however, was unaffected by the srtA mutation. The M1 genome sequence contains a second open reading frame with a motif characteristic of sortase proteins. Inactivation of this gene (designated srtB) in strain JRS4 affected the surface localization of T6 but not M6, protein F, ScpA, or GRAB. This phenotype was complemented by srtB in trans. An srtA probe hybridized with DNA from all GAS strains tested (M types 1, 3, 4, 5, 6, 18, 22, and 50 and nontypeable strain 64/14) and from streptococcal groups C and G, while srtB hybridized with DNA from only a few GAS strains. We conclude that srtA and srtB encode sortase enzymes required for anchoring different subsets of proteins to the cell wall. It seems likely that the multiple sortase homologs in the genomes of other gram-positive bacteria have a similar substrate-specific role.
* Corresponding author. Mailing address: Department of Microbiology and Immunology, 3001 Rollins Research Center, Emory University School of Medicine, Atlanta, GA 30322. Phone: (404) 727-0402. Fax: (404) 727-8999. E-mail:
scott{at}microbio.emory.edu.
Journal of Bacteriology, April 2002, p. 2181-2191, Vol. 184, No. 8
0021-9193/02/$04.00+0 DOI: 10.1128/JB.184.8.2181-2191.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Kline, K. A., Kau, A. L., Chen, S. L., Lim, A., Pinkner, J. S., Rosch, J., Nallapareddy, S. R., Murray, B. E., Henriques-Normark, B., Beatty, W., Caparon, M. G., Hultgren, S. J.
(2009). Mechanism for Sortase Localization and the Role of Sortase Localization in Efficient Pilus Assembly in Enterococcus faecalis. J. Bacteriol.
191: 3237-3247
[Abstract]
[Full Text]
-
Race, P. R., Bentley, M. L., Melvin, J. A., Crow, A., Hughes, R. K., Smith, W. D., Sessions, R. B., Kehoe, M. A., McCafferty, D. G., Banfield, M. J.
(2009). Crystal Structure of Streptococcus pyogenes Sortase A: IMPLICATIONS FOR SORTASE MECHANISM. J. Biol. Chem.
284: 6924-6933
[Abstract]
[Full Text]
-
Nakata, M., Koller, T., Moritz, K., Ribardo, D., Jonas, L., McIver, K. S., Sumitomo, T., Terao, Y., Kawabata, S., Podbielski, A., Kreikemeyer, B.
(2009). Mode of Expression and Functional Characterization of FCT-3 Pilus Region-Encoded Proteins in Streptococcus pyogenes Serotype M49. Infect. Immun.
77: 32-44
[Abstract]
[Full Text]
-
Raz, A., Fischetti, V. A.
(2008). Sortase A localizes to distinct foci on the Streptococcus pyogenes membrane. Proc. Natl. Acad. Sci. USA
105: 18549-18554
[Abstract]
[Full Text]
-
LeMieux, J., Woody, S., Camilli, A.
(2008). Roles of the Sortases of Streptococcus pneumoniae in Assembly of the RlrA Pilus. J. Bacteriol.
190: 6002-6013
[Abstract]
[Full Text]
-
Nobbs, A. H., Rosini, R., Rinaudo, C. D., Maione, D., Grandi, G., Telford, J. L.
(2008). Sortase A Utilizes an Ancillary Protein Anchor for Efficient Cell Wall Anchoring of Pili in Streptococcus agalactiae. Infect. Immun.
76: 3550-3560
[Abstract]
[Full Text]
-
Rosch, J. W., Vega, L. A., Beyer, J. M., Lin, A., Caparon, M. G.
(2008). The Signal Recognition Particle Pathway Is Required for Virulence in Streptococcus pyogenes. Infect. Immun.
76: 2612-2619
[Abstract]
[Full Text]
-
Bentley, M. L., Lamb, E. C., McCafferty, D. G.
(2008). Mutagenesis Studies of Substrate Recognition and Catalysis in the Sortase A Transpeptidase from Staphylococcus aureus. J. Biol. Chem.
283: 14762-14771
[Abstract]
[Full Text]
-
DeDent, A. C., McAdow, M., Schneewind, O.
(2007). Distribution of Protein A on the Surface of Staphylococcus aureus. J. Bacteriol.
189: 4473-4484
[Abstract]
[Full Text]
-
Bentley, M. L., Gaweska, H., Kielec, J. M., McCafferty, D. G.
(2007). Engineering the Substrate Specificity of Staphylococcus aureus Sortase A: THE beta6/beta7 LOOP FROM SrtB CONFERS NPQTN RECOGNITION TO SrtA. J. Biol. Chem.
282: 6571-6581
[Abstract]
[Full Text]
-
Lizano, S., Luo, F., Bessen, D. E.
(2007). Role of Streptococcal T Antigens in Superficial Skin Infection. J. Bacteriol.
189: 1426-1434
[Abstract]
[Full Text]
-
Kratovac, Z., Manoharan, A., Luo, F., Lizano, S., Bessen, D. E.
(2007). Population Genetics and Linkage Analysis of Loci within the FCT Region of Streptococcus pyogenes. J. Bacteriol.
189: 1299-1310
[Abstract]
[Full Text]
-
Podbielski, A.
(2007). Flexible Architecture of the Streptococcus pyogenes FCT Genome Region: Finally the Clue for Understanding Purulent Skin Diseases and Long-Term Persistence?{triangledown}. J. Bacteriol.
189: 1181-1184
[Full Text]
-
Swierczynski, A., Ton-That, H.
(2006). Type III Pilus of Corynebacteria: Pilus Length Is Determined by the Level of Its Major Pilin Subunit.. J. Bacteriol.
188: 6318-6325
[Abstract]
[Full Text]
-
Marraffini, L. A., DeDent, A. C., Schneewind, O.
(2006). Sortases and the Art of Anchoring Proteins to the Envelopes of Gram-Positive Bacteria. Microbiol. Mol. Biol. Rev.
70: 192-221
[Abstract]
[Full Text]
-
Gaspar, A. H., Ton-That, H.
(2006). Assembly of Distinct Pilus Structures on the Surface of Corynebacterium diphtheriae. J. Bacteriol.
188: 1526-1533
[Abstract]
[Full Text]
-
Lee, S. G., Fischetti, V. A.
(2006). Purification and Characterization of LPXTGase from Staphylococcus aureus: the Amino Acid Composition Mirrors That Found in the Peptidoglycan. J. Bacteriol.
188: 389-398
[Abstract]
[Full Text]
-
Davison, S., Couture-Tosi, E., Candela, T., Mock, M., Fouet, A.
(2005). Identification of the Bacillus anthracis {gamma} Phage Receptor. J. Bacteriol.
187: 6742-6749
[Abstract]
[Full Text]
-
Boekhorst, J., de Been, M. W. H. J., Kleerebezem, M., Siezen, R. J.
(2005). Genome-Wide Detection and Analysis of Cell Wall-Bound Proteins with LPxTG-Like Sorting Motifs. J. Bacteriol.
187: 4928-4934
[Abstract]
[Full Text]
-
Gaspar, A. H., Marraffini, L. A., Glass, E. M., DeBord, K. L., Ton-That, H., Schneewind, O.
(2005). Bacillus anthracis Sortase A (SrtA) Anchors LPXTG Motif-Containing Surface Proteins to the Cell Wall Envelope. J. Bacteriol.
187: 4646-4655
[Abstract]
[Full Text]
-
Lalioui, L., Pellegrini, E., Dramsi, S., Baptista, M., Bourgeois, N., Doucet-Populaire, F., Rusniok, C., Zouine, M., Glaser, P., Kunst, F., Poyart, C., Trieu-Cuot, P.
(2005). The SrtA Sortase of Streptococcus agalactiae Is Required for Cell Wall Anchoring of Proteins Containing the LPXTG Motif, for Adhesion to Epithelial Cells, and for Colonization of the Mouse Intestine. Infect. Immun.
73: 3342-3350
[Abstract]
[Full Text]
-
Pajunen, M. I., Pulliainen, A. T., Finne, J., Savilahti, H.
(2005). Generation of transposon insertion mutant libraries for Gram-positive bacteria by electroporation of phage Mu DNA transposition complexes. Microbiology
151: 1209-1218
[Abstract]
[Full Text]
-
Barnett, T. C., Patel, A. R., Scott, J. R.
(2004). A Novel Sortase, SrtC2, from Streptococcus pyogenes Anchors a Surface Protein Containing a QVPTGV Motif to the Cell Wall. J. Bacteriol.
186: 5865-5875
[Abstract]
[Full Text]
-
Zong, Y., Bice, T. W., Ton-That, H., Schneewind, O., Narayana, S. V. L.
(2004). Crystal Structures of Staphylococcus aureus Sortase A and Its Substrate Complex. J. Biol. Chem.
279: 31383-31389
[Abstract]
[Full Text]
-
Comfort, D., Clubb, R. T.
(2004). A Comparative Genome Analysis Identifies Distinct Sorting Pathways in Gram-Positive Bacteria. Infect. Immun.
72: 2710-2722
[Abstract]
[Full Text]
-
Bierne, H., Garandeau, C., Pucciarelli, M. G., Sabet, C., Newton, S., Garcia-del Portillo, F., Cossart, P., Charbit, A.
(2004). Sortase B, a New Class of Sortase in Listeria monocytogenes. J. Bacteriol.
186: 1972-1982
[Abstract]
[Full Text]
-
Weiss, W. J., Lenoy, E., Murphy, T., Tardio, L., Burgio, P., Projan, S. J., Schneewind, O., Alksne, L.
(2004). Effect of srtA and srtB gene expression on the virulence of Staphylococcus aureus in animal models of infection. J Antimicrob Chemother
53: 480-486
[Abstract]
[Full Text]
-
Kharat, A. S., Tomasz, A.
(2003). Inactivation of the srtA Gene Affects Localization of Surface Proteins and Decreases Adhesion of Streptococcus pneumoniae to Human Pharyngeal Cells In Vitro. Infect. Immun.
71: 2758-2765
[Abstract]
[Full Text]
-
Voyich, J. M., Sturdevant, D. E., Braughton, K. R., Kobayashi, S. D., Lei, B., Virtaneva, K., Dorward, D. W., Musser, J. M., DeLeo, F. R.
(2003). Genome-wide protective response used by group A Streptococcus to evade destruction by human polymorphonuclear leukocytes. Proc. Natl. Acad. Sci. USA
100: 1996-2001
[Abstract]
[Full Text]
-
Jeng, A., Sakota, V., Li, Z., Datta, V., Beall, B., Nizet, V.
(2003). Molecular Genetic Analysis of a Group A Streptococcus Operon Encoding Serum Opacity Factor and a Novel Fibronectin-Binding Protein, SfbX. J. Bacteriol.
185: 1208-1217
[Abstract]
[Full Text]
-
Lee, S. F., Boran, T. L.
(2003). Roles of Sortase in Surface Expression of the Major Protein Adhesin P1, Saliva-Induced Aggregation and Adherence, and Cariogenicity of Streptococcus mutans. Infect. Immun.
71: 676-681
[Abstract]
[Full Text]