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10 - The Mobile Genetic Elements of Staphylococcus aureus

from PART III - Paradigms of Bacterial Evolution

Published online by Cambridge University Press:  16 September 2009

By
Richard P. Novick
Edited by
Michael Hensel  and
Herbert Schmidt
Michael Hensel
Affiliation:
Friedrich-Alexander-Universität Erlangen-Nürnberg, Germany
Herbert Schmidt
Affiliation:
Universität Hohenheim, Stuttgart
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Summary

INTRODUCTION

Like most eubacteria, S. aureus possesses a variety of mobile genetic elements (MGEs) that contribute in major ways to pathogenesis and its evolution. In addition to the typical MGEs carried by most bacteria, that is, prophages, transposons, and plasmids, S. aureus possesses two types of novel elements that have not been described for other bacteria, namely the superantigen-encoding pathogenicity islands and the resistance-encoding SCCmec elements. In this chapter, the general properties of these various MGEs are summarized, with special emphasis on the two novel types and on their contributions to pathogenesis and its evolution.

MOLECULAR GENETICS OF THE STAPHYLOCOCCAL MGEs

Plasmids

For a comprehensive review of plasmid origins and interactions, see Firth and Skurray (2006). Staphylococcal plasmids range in size from 1.2 to more than 100 kb; all known staphylococcal plasmids are circular duplex DNA, using either of the two standard modes of replication, theta and rolling circle (RC), with the latter being used principally by those of less than 10 kb, and the former by those larger, though this is only an approximate dividing line. As with all other plasmids, replication of staphylococcal plasmids is negatively autoregulated. For the known small RC plasmids, this is accomplished by cis-encoded antisense RNAs, sometimes with the assistance of small proteins. Theta plasmids of the pSK41/pGO1 family also appear to use an antisense mechanism.

Type
Chapter
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Horizontal Gene Transfer in the Evolution of Pathogenesis , pp. 237 - 272
Publisher: Cambridge University Press
Print publication year: 2008

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References

Arnold, H. P., She, Q., Phan, H., et al. (1999). The genetic element pSSVx of the extremely thermophilic crenarchaeon Sulfolobus is a hybrid between a plasmid and a virus. Mol Microbiol, 34, 217–26.CrossRefGoogle ScholarPubMed
Baba, T., Takeuchi, F., Kuroda, M., et al. (2002). Genome and virulence determinants of high virulence community-acquired MRSA. Lancet, 359, 1819–27.CrossRefGoogle ScholarPubMed
Bensing, B. A., Lopez, J. A., and Sullam, P. M. (2004). The Streptococcus gordonii surface proteins GspB and Hsa mediate binding to sialylated carbohydrate epitopes on the platelet membrane glycoprotein Ibalpha. Infect Immun, 72, 6528–37.CrossRefGoogle ScholarPubMed
Berg, T., Firth, N., Apisiridej, S., et al. (1998). Complete nucleotide sequence of pSK41: evolution of staphylococcal conjugative multiresistance plasmids. J Bacteriol, 180, 4350–9.Google ScholarPubMed
Birch, P., and Khan, S. A. (1992). Replication of single-stranded plasmid pT181 DNA in vitro. Proc Natl Acad Sci USA, 89, 290–4.CrossRefGoogle ScholarPubMed
Chatterjee, A. N. (1969). Use of bacteriophage-resistant mutants to study the nature of the bacteriophage receptor site of Staphylococcus aureus. J Bacteriol, 98, 519–27.Google Scholar
Chongtrakool, P., Ito, T., Ma, X. X., et al. (2006). Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: a proposal for a new nomenclature for SCCmec elements. Antimicrob Agents Chemother, 50, 1001–12.CrossRefGoogle ScholarPubMed
Coleman, D. C., Sullivan, D. J., Russell, R. J., et al. (1989). Staphylococcus aureus bacteriophages mediating the simultaneous lysogenic conversion of β-lysin, staphylokinase and enterotoxin A: molecular mechanism of triple conversion. J Gen Microbiol, 135, 1679–97.Google ScholarPubMed
Diep, B. A., Gill, S. R., Chang, R. F., et al. (2006). Complete genome sequence of USA300, an epidemic community-acquired methicillin-resistant Staphylococcus aureus strain. Lancet, 367, 731–9.CrossRefGoogle Scholar
Firth, N., and Skurray, R. A. (1998). Mobile elements in the evolution and spread of multiple-drug resistance in staphylococci. Drug Resist Updates, 1, 49–58.CrossRefGoogle ScholarPubMed
Firth, N., and Skurray, R. A. (2006). Genetics: accessory elements and genetic exchange. In Fischetti, V. A., Novick, R. P., Ferretti, J. J., Portnoy, D. A., and Rood, J. I. (Eds.). Gram-positive pathogens (2nd ed.). Washington, DC: ASM Press.Google Scholar
Firth, N., Apisiridej, S., Berg, T., et al. (2000). Replication of staphylococcal multiresistance plasmids. J Bacteriol, 182, 2170–8.CrossRefGoogle ScholarPubMed
Fitzgerald, J. R., Monday, S. R., Foster, T. J., et al. (2001). Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol, 183, 63–70.CrossRefGoogle ScholarPubMed
Gennaro, M. L., Kornblum, J., and Novick, R. P. (1987). A site-specific recombination function in Staphylococcus aureus plasmids. J Bacteriol, 169, 2601–10.CrossRefGoogle ScholarPubMed
Gill, S. R., Fouts, D. E., Archer, G. L., et al. (2005). Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol, 187, 2426–38.CrossRefGoogle Scholar
Gillet, Y., Issartel, B., Vanhems, P., et al. (2002). Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet, 359, 753–9.CrossRefGoogle ScholarPubMed
Groisman, E. A., and Ochman, H. (1996). Pathogenicity islands: bacterial evolution in quantum leaps. Cell, 87, 791–4.CrossRefGoogle ScholarPubMed
Gruss, A. D., Ross, H. F., and Novick, R. P. (1987). Functional analysis of a palindromic sequence required for normal replication of several staphylococcal plasmids. Proc Natl Acad Sci USA, 84, 2165–9.CrossRefGoogle ScholarPubMed
Highlander, S. K., and Novick, R. P. (1990). Mutational and physiological analyses of plasmid pT181 functions expressing incompatibility. Plasmid, 23, 1–15.CrossRefGoogle ScholarPubMed
Hochhut, B., Dobrindt, U., and Hacker, J. (2005). Pathogenicity islands and their role in bacterial virulence and survival. Contrib Microbiol, 12, 234–54.CrossRefGoogle Scholar
Holden, M. T., Feil, E. J., Lindsay, J. A., et al. (2004). Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci USA, 101, 9786–91.CrossRefGoogle ScholarPubMed
Johnson, L. B., Saeed, S., Pawlak, J., Manzor, O., and Saravolatz, L. D. (2006). Clinical and laboratory features of community-associated methicillin-resistant Staphylococcus aureus: is it really new?Infect Control Hosp Epidemiol, 27, 133–8.CrossRefGoogle ScholarPubMed
Khan, S. A. (2005). Plasmid rolling-circle replication: highlights of two decades of research. Plasmid, 53, 126–36.CrossRefGoogle Scholar
King, M. D., Humphrey, B. J., Wang, Y. F., et al. (2006). Emergence of community-acquired methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections. Ann Intern Med, 144, 309–17.CrossRefGoogle ScholarPubMed
Kramer, M. G., Espinosa, M., Misra, T. K., and Khan, S. A. (1998). Lagging strand replication of rolling-circle plasmids: specific recognition of the ssoA-type origins in different gram-positive bacteria. Proc Natl Acad Sci USA, 95, 10505–10.CrossRefGoogle ScholarPubMed
Krolewski, J. J., Murphy, E., Novick, R. P., and Rush, M. G. (1981). Site-specificity of the chromosomal insertion of Staphylococcus aureus transposon Tn554. J Mol Biol, 152, 19–33.CrossRefGoogle ScholarPubMed
Kuroda, M., Ohta, T., Uchiyama, I., et al. (2001). Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet, 357, 1225–40.CrossRefGoogle Scholar
Kuroda, M., Yamashita, A., Hirakawa, H., et al. (2005). Whole genome sequence of Staphylococcus saprophyticus reveals the pathogenesis of uncomplicated urinary tract infection. Proc Natl Acad Sci USA, 102, 13272–7.CrossRefGoogle ScholarPubMed
Kwan, T., Liu, J., Dubow, M., Gros, P., and Pelletier, J. (2005). The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc Natl Acad Sci USA, 102, 5174–9.CrossRefGoogle ScholarPubMed
Lee, C. Y., and Iandolo, J. J. (1986). Lysogenic conversion of staphylococcal lipase caused by insertion of the bacteriophage L54a genome into the lipase structural gene. J Bacteriol, 166, 385–91.CrossRefGoogle ScholarPubMed
Lina, G., Piemont, Y., Godail-Gamot, F., et al. (1999). Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis, 29, 1128–32.CrossRefGoogle ScholarPubMed
Lindqvist, B. H., Deho, G., and Calendar, R. (1993). Mechanisms of genome propagation and helper exploitation by satellite phage P4. Microbiol Rev, 57, 683–702.Google ScholarPubMed
Lindsay, J. A., Ruzin, A., Ross, H. F., Kurepina, N., and Novick, R. P. (1998). The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol, 29, 527–43.CrossRefGoogle ScholarPubMed
Lyon, B. R., and Skurray, R. (1987). Antimicrobial resistance of Staphylococcus aureus: genetic basis. Microbiol Rev, 51, 88–134.Google ScholarPubMed
Macrina, F. L., and Archer, G. L. (1993). Conjugation and broad host range plasmids in streptococci and staphylococci. In Clewell, D. B. (Ed.). Bacterial conjugation. New York: Plenum.Google Scholar
Marrack, P., Winslow, G. M., Choi, Y., et al. (1993). The bacterial and mouse mammary tumor virus superantigens; two different families of proteins with the same functions. Immunol Rev, 131, 79–92.CrossRefGoogle ScholarPubMed
Musser, J. M., Schlievert, P. M., Chow, A. W., et al. (1990). A single clone of Staphylococcus aureus causes the majority of cases of toxic shock syndrome. Proc Natl Acad Sci USA, 87, 225–9.CrossRefGoogle ScholarPubMed
Nakayama, J., Igarashi, S., Nagasawa, H., et al. (1996). Isolation and structure of staph-cAM373 produced by Staphylococcus aureus that induces conjugal transfer of Enterococcus faecalis plasmid pAM373. Biosci Biotechnol Biochem, 60, 1038–9.CrossRefGoogle ScholarPubMed
Narita, S., Kaneko, J., Chiba, J., et al. (2001). Phage conversion of Panton-Valentine leukocidin in Staphylococcus aureus: molecular analysis of a PVL-converting phage, phiSLT. Gene, 268, 195–206.CrossRefGoogle ScholarPubMed
Nimmo, G. R., Coombs, G. W., Pearson, J. C., et al. (2006). Methicillin-resistant Staphylococcus aureus in the Australian community: an evolving epidemic. Med J Aust, 184, 384–8.Google ScholarPubMed
Novick, R. (1976). Plasmid-protein relaxation complexes in Staphylococcus aureus. J Bacteriol, 127, 1177–87.Google ScholarPubMed
Novick, R. P. (1967). Mutations affecting replication and maintenance of penicillinase plasmids in S. aureus. Paper presented at the Fifth International Congress of Chemotherapy, Vienna.
Novick, R. P. (1980). Plasmids. Sci Am, 243, 102–4, 6, 10 passim.CrossRefGoogle ScholarPubMed
Novick, R. P. (1987). Plasmid incompatibility. Microbiol Rev, 51, 381–95.Google ScholarPubMed
Novick, R. P. (2003). Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid, 49, 93–105.CrossRefGoogle ScholarPubMed
Novick, R. P., Iordanescu, S., Projan, S. J., Kornblum, J., and Edelman, I. (1989). pT181 plasmid replication is regulated by a countertranscript-driven transcriptional attenuator. Cell, 59, 395–404.CrossRefGoogle ScholarPubMed
Novick, R. P., Schlievert, P., and Ruzin, A. (2001). Pathogenicity and resistance islands of staphylococci. Microb Infect, 3, 585–94.CrossRefGoogle ScholarPubMed
Oliveira, D. C., and Lencastre, H. (2002). Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother, 46, 2155–61.CrossRefGoogle ScholarPubMed
Paulsen, I. T., Firth, N., and Skurray, R. A. (1997). Resistance to antimicrobial agents other than β-lactams. In Crossley, K. B., and Archer, G. L. (Eds.). The staphylococci in human disease. New York: Churchill Livingstone.Google Scholar
Projan, S. J., and Archer, G. L. (1989). Mobilization of the relaxable Staphylococcus aureus plasmid pC221 by the conjugative plasmid pG01 involves three pC221 loci. J Bacteriol, 171, 1841–5.CrossRefGoogle Scholar
Rasooly, A., and Novick, R. P. (1993). Replication-specific inactivation of the pT181 plasmid initiator protein. Science, 262, 1048–50.CrossRefGoogle ScholarPubMed
Ruzin, A., Lindsay, J., and Novick, R. P. (2001). Molecular genetics of SaPI1 – a mobile pathogenicity island in Staphylococcus aureus. Mol Microbiol, 41, 365–77.CrossRefGoogle ScholarPubMed
Stout, V. G., and Iandolo, J. J. (1990). Chromosomal gene transfer during conjugation by Staphylococcus aureus is mediated by transposon-facilitated mobilization. J Bacteriol, 172, 6148–50.CrossRefGoogle ScholarPubMed
Takeuchi, F., Watanabe, S., Baba, T., et al. (2005). Whole-genome sequencing of Staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol, 187, 7292–308.CrossRefGoogle ScholarPubMed
Thomas, W. D., and Archer, G. L. (1989). Identification and cloning of the conjugative transfer region of the S. aureus plasmid pG01. J Bacteriol, 171, 684–91.CrossRefGoogle Scholar
Timmis, K., Cabello, F., and Cohen, S. N. (1975). Cloning, isolation, and characterization of replication regions of complex plasmid genomes. Proc Natl Acad Sci USA, 72, 2242–6.CrossRefGoogle ScholarPubMed
Ubeda, C., Tormo, M. A., Cucarella, C., et al. (2003). Sip, an integrase protein with excision, circularization and integration activities, defines a new family of mobile Staphylococcus aureus pathogenicity islands. Mol Microbiol, 49, 193–210.CrossRefGoogle ScholarPubMed
Udo, E. E., and Jacob, L. E. (1998). Conjugative transfer of high-level mupirocin resistance and the mobilization of non-conjugative plasmids in Staphylococcus aureus. Microb Drug Resist, 4, 185–93.CrossRefGoogle ScholarPubMed
Waldor, M. K., and Friedman, D. I. (2005). Phage regulatory circuits and virulence gene expression. Curr Opin Microbiol, 8, 459–65.CrossRefGoogle ScholarPubMed
Weigel, L. M., Clewell, D. B., Gill, S. R., et al. (2003). Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science, 302, 1569–71.CrossRefGoogle ScholarPubMed
Winkler, K. C., Wart, J. D., and Grootsen, C. (1965). Lysogenic conversion of staphylococci to loss of β-toxin. J Gen Microbiol, 39, 321–33.CrossRefGoogle ScholarPubMed
Wu, S. W., Lencastre, H., and Tomasz, A. (1999). The Staphylococcus aureus transposon Tn551: complete nucleotide sequence and transcriptional analysis of the expression of the erythromycin resistance gene. Microb Drug Resist, 5, 1–7.CrossRefGoogle ScholarPubMed
Zhang, X., McDaniel, A. D., Wolf, L. E., et al. (2000). Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice. J Infect Dis, 181, 664–70.CrossRefGoogle ScholarPubMed
Zhang, Y. Q., Ren, S. X., Li, H. L., et al. (2003). Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol Microbiol, 49, 1577–93.CrossRefGoogle Scholar
Zou, D., Kaneko, J., Narita, S., and Kamio, Y. (2000). Prophage, phiPV83-pro, carrying Panton-Valentine leukocidin genes, on the Staphylococcus aureus P83 chromosome: comparative analysis of the genome structures of phiPV83-pro, phiPVL, phi11, and other phages. Biosci Biotechnol Biochem, 64, 2631–43.CrossRefGoogle ScholarPubMed

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