Previous Article | Next Article 
Journal of Bacteriology, December 2005, p. 8312-8321, Vol. 187, No. 24
0021-9193/05/$08.00+0 doi:10.1128/JB.187.24.8312-8321.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.
Evolutionary Genetics of the Accessory Gene Regulator (agr) Locus in Staphylococcus aureus
D. Ashley Robinson,1*
Alastair B. Monk,2
Jessica E. Cooper,3
Edward J. Feil,3 and
Mark C. Enright4
New York Medical College, Department of Microbiology and Immunology, Valhalla, New York 10595,1
Virginia Commonwealth University, Department of Internal Medicine, Richmond, Virginia 23298,2
University of Bath, Department of Biology and Biochemistry, Bath, United Kingdom BA2 7AY,3
Imperial College London, Department of Infectious Disease Epidemiology, London, United Kingdom W2 1PG4
Received 20 July 2005/
Accepted 4 October 2005
The accessory gene regulator (agr) locus influences the expression of many virulence genes in the human pathogen Staphylococcus aureus. Four allelic groups of agr, which generally inhibit the regulatory activity of each other, have been identified within the species. Interference in virulence gene expression caused by different agr groups has been suggested to be a mechanism for isolating bacterial populations and a fundamental basis for subdividing the species. To test the hypothesis that the species is phylogenetically structured according to agr groups, we mapped agr groups onto a clone phylogeny inferred from partial sequences of 14 genes from 27 genetically diverse strains. Shimodaira-Hasegawa and parametric bootstrap tests rejected the hypotheses that the species is subdivided into three or five monophyletic agr groups but failed to reject the hypothesis that the species is subdivided into two groups that each consist of multiple clonal complexes and multiple agr groups. Additional evidence for agr recombination is found from clustered polymorphisms in complete agr sequences. However, agr recombination has not occurred frequently or randomly through time, because the topology and branch lengths of the clone phylogeny are reflected within each agr group. To account for these observations, we propose a new evolutionary model that involves a genetically polymorphic ancestral population of S. aureus that horizontally transferred agr groups between two subspecies groups near the time that these subspecies groups diverged.
* Corresponding author. Mailing address: New York Medical College, Department of Microbiology and Immunology, Valhalla, NY 10595. Phone: (914) 594-4973. Fax: (914) 594-4176. E-mail:
ashley_robinson{at}nymc.edu.
Supplemental material for this article may be found at http://jb.asm.org/.
Journal of Bacteriology, December 2005, p. 8312-8321, Vol. 187, No. 24
0021-9193/05/$08.00+0 doi:10.1128/JB.187.24.8312-8321.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Smyth, D. S., Robinson, D. A.
(2009). Integrative and Sequence Characteristics of a Novel Genetic Element, ICE6013, in Staphylococcus aureus. J. Bacteriol.
191: 5964-5975
[Abstract]
[Full Text]
-
Smyth, D. S., Feil, E. J., Meaney, W. J., Hartigan, P. J., Tollersrud, T., Fitzgerald, J. R., Enright, M. C., Smyth, C. J.
(2009). Molecular genetic typing reveals further insights into the diversity of animal-associated Staphylococcus aureus. J Med Microbiol
58: 1343-1353
[Abstract]
[Full Text]
-
Sugiyama, Y., Okii, K., Murakami, Y., Yokoyama, T., Takesue, Y., Ohge, H., Sueda, T., Hiyama, E.
(2009). Changes in the agr Locus Affect Enteritis Caused by Methicillin-Resistant Staphylococcus aureus. J. Clin. Microbiol.
47: 1528-1535
[Abstract]
[Full Text]
-
Perez-Vazquez, M., Vindel, A., Marcos, C., Oteo, J., Cuevas, O., Trincado, P., Bautista, V., Grundmann, H., Campos, J., on behalf of the EARSS Spain spa-typing Group,
(2009). Spread of invasive Spanish Staphylococcus aureus spa-type t067 associated with a high prevalence of the aminoglycoside-modifying enzyme gene ant(4')-Ia and the efflux pump genes msrA/msrB. J Antimicrob Chemother
63: 21-31
[Abstract]
[Full Text]
-
Ruimy, R., Maiga, A., Armand-Lefevre, L., Maiga, I., Diallo, A., Koumare, A. K., Ouattara, K., Soumare, S., Gaillard, K., Lucet, J.-C., Andremont, A., Feil, E. J.
(2008). The Carriage Population of Staphylococcus aureus from Mali Is Composed of a Combination of Pandemic Clones and the Divergent Panton-Valentine Leukocidin-Positive Genotype ST152. J. Bacteriol.
190: 3962-3968
[Abstract]
[Full Text]
-
Collery, M. M., Smyth, D. S., Twohig, J. M., Shore, A. C., Coleman, D. C., Smyth, C. J.
(2008). Molecular typing of nasal carriage isolates of Staphylococcus aureus from an Irish university student population based on toxin gene PCR, agr locus types and multiple locus, variable number tandem repeat analysis. J Med Microbiol
57: 348-358
[Abstract]
[Full Text]
-
Bannoehr, J., Ben Zakour, N. L., Waller, A. S., Guardabassi, L., Thoday, K. L., van den Broek, A. H. M., Fitzgerald, J. R.
(2007). Population Genetic Structure of the Staphylococcus intermedius Group: Insights into agr Diversification and the Emergence of Methicillin-Resistant Strains. J. Bacteriol.
189: 8685-8692
[Abstract]
[Full Text]
-
Holtfreter, S., Grumann, D., Schmudde, M., Nguyen, H. T. T., Eichler, P., Strommenger, B., Kopron, K., Kolata, J., Giedrys-Kalemba, S., Steinmetz, I., Witte, W., Broker, B. M.
(2007). Clonal Distribution of Superantigen Genes in Clinical Staphylococcus aureus Isolates. J. Clin. Microbiol.
45: 2669-2680
[Abstract]
[Full Text]
-
Monk, A. B., Archer, G. L.
(2007). Use of Outer Surface Protein Repeat Regions for Improved Genotyping of Staphylococcus epidermidis. J. Clin. Microbiol.
45: 730-735
[Abstract]
[Full Text]
-
Buzzola, F. R., Alvarez, L. P., Tuchscherr, L. P. N., Barbagelata, M. S., Lattar, S. M., Calvinho, L., Sordelli, D. O.
(2007). Differential Abilities of Capsulated and Noncapsulated Staphylococcus aureus Isolates from Diverse agr Groups To Invade Mammary Epithelial Cells. Infect. Immun.
75: 886-891
[Abstract]
[Full Text]
-
Francois, P., Koessler, T., Huyghe, A., Harbarth, S., Bento, M., Lew, D., Etienne, J., Pittet, D., Schrenzel, J.
(2006). Rapid Staphylococcus aureus agr Type Determination by a Novel Multiplex Real-Time Quantitative PCR Assay.. J. Clin. Microbiol.
44: 1892-1895
[Abstract]
[Full Text]
-
Cooper, J. E., Feil, E. J.
(2006). The phylogeny of Staphylococcus aureus - which genes make the best intra-species markers?. Microbiology
152: 1297-1305
[Abstract]
[Full Text]