Evolution of hypervirulence by a MRSA clone through acquisition of a transposable element

Molecular Microbiology

Volumn 93, Issue 4, 2014, Pages 664-681

  Benson, Meredith A ^a,i   Ohneck, Elizabeth A ^a   Ryan, Chanelle ^b   Alonzo, Francis ^a   Smith, Hannah ^b   Narechania, Apurva ^c   Kolokotronis, Sergios Orestis ^d   Satola, Sarah W ^e,f   Uhlemann, Anne Catrin ^g   Sebra, Robert ^h   Deikus, Gintaras ^h   Shopsin, Bo ^a   Planet, Paul J ^b,c   Torres, Victor J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

^d FORDHAM UNIVERSITY   (United States)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f ATLANTA VA MEDICAL CENTER   (United States)

^g Department of Medicine   (United States)

^h MOUNT SINAI HOSPITAL   (United States)

ⁱ BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIN; PROTEIN ROT; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL DNA; BACTERIAL PROTEIN; BACTERIAL TOXIN; REPRESSOR PROTEIN; ROT PROTEIN, STAPHYLOCOCCUS AUREUS; TRANSPOSON;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; GENE CONTROL; GENE DOSAGE; GENE EXPRESSION; GENE INSERTION; GENETIC CONSERVATION; GENOME ANALYSIS; HORIZONTAL GENE TRANSFER; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REPRESSOR GENE; TRANSCRIPTION REGULATION; TRANSPOSON; BIOSYNTHESIS; CHEMISTRY; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MOLECULAR EVOLUTION; MOLECULAR GENETICS; VIRULENCE;

METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; BACTERIAL TOXINS; DNA TRANSPOSABLE ELEMENTS; DNA, BACTERIAL; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; RECOMBINATION, GENETIC; REPRESSOR PROTEINS; SEQUENCE ANALYSIS, DNA; VIRULENCE; VIRULENCE FACTORS;

EID: 84925884174     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12682     Document Type: Article

References (59)

1. Alonzo, F., 3rd, Benson, M.A., Chen, J., Novick, R.P., Shopsin, B., and Torres, V.J. (2012) Staphylococcus aureus leucocidin ED contributes to systemic infection by targeting neutrophils and promoting bacterial growth in vivo. Mol Microbiol 83: 423-435.
2. Bae, T., and Schneewind, O. (2006) Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55: 58-63.
3. Benson, M.A., Lilo, S., Wasserman, G.A., Thoendel, M., Smith, A., Horswill, A.R., etal. (2011) Staphylococcus aureus regulates the expression and production of the staphylococcal superantigen-like secreted proteins in a Rot-dependent manner. Mol Microbiol 81: 659-675.
4. Benson, M.A., Lilo, S., Nygaard, T., Voyich, J.M., and Torres, V.J. (2012) Rot and SaeRS cooperate to activate expression of the staphylococcal superantigen-like exoproteins. J Bacteriol 194: 4355-4365.
5. Boisset, S., Geissmann, T., Huntzinger, E., Fechter, P., Bendridi, N., Possedko, M., etal. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21: 1353-1366.
6. Bubeck Wardenburg, J., Bae, T., Otto, M., Deleo, F.R., and Schneewind, O. (2007) Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 13: 1405-1406.
7. Chin, C., Alexander, D.H., Marks, P., Klammer, A.A., Drake, J., Heiner, C., etal. (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10: 563-569.
8. Cocchi, P., Cariani, L., Favari, F., Lambiase, A., Fiscarelli, E., Gioffre, F.V., etal. (2011) Molecular epidemiology of meticillin-resistant Staphylococcus aureus in Italian cystic fibrosis patients: a national overview. J Cyst Fibros 10: 407-411.
9. Conlon, K.M., Humphreys, H., and O'Gara, J.P. (2004) Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis. J Bacteriol 186: 6208-6219.
10. Diep, B.A., Carleton, H.A., Chang, R.F., Sensabaugh, G.F., and Perdreau-Remington, F. (2006) Roles of 34 virulence genes in the evolution of hospital- and community-associated strains of methicillin-resistant Staphylococcus aureus. J Infect Dis 193: 1495-1503.
11. DuMont, A.L., Nygaard, T.K., Watkins, R.L., Smith, A., Kozhaya, L., Kreiswirth, B.N., etal. (2011) Characterization of a new cytotoxin that contributes to Staphylococcus aureus pathogenesis. Mol Microbiol 79: 814-825.
12. DuMont, A.L., Yoong, P., Day, C.J., Alonzo, F., 3rd, McDonald, W.H., Jennings, M.P., and Torres, V.J. (2013a) Staphylococcus aureus LukAB cytotoxin kills human neutrophils by targeting the CD11b subunit of the integrin Mac-1. Proc Natl Acad Sci USA 110: 10794-10799.
13. DuMont, A.L., Yoong, P., Surewaard, B.G., Benson, M.A., Nijland, R., van Strijp, J.A., and Torres, V.J. (2013b) Staphylococcus aureus elaborates leukocidin AB to mediate escape from within human neutrophils. Infect Immun 81: 1830-1841.
14. Edgeworth, J.D., Yadegarfar, G., Pathak, S., Batra, R., Cockfield, J.D., Wyncoll, D., etal. (2007) An outbreak in an intensive care unit of a strain of methicillin-resistant Staphylococcus aureus sequence type 239 associated with an increased rate of vascular access device-related bacteremia. Clin Infect Dis 44: 493-501.
15. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
16. Geisinger, E., Adhikari, R.P., Jin, R., Ross, H.F., and Novick, R.P. (2006) Inhibition of rot translation by RNAIII, a key feature of agr function. Mol Microbiol 61: 1038-1048.
17. Gillespie, M.T., Lyon, B.R., Messerotti, L.J., and Skurray, R.A. (1987) Chromosome- and plasmid-mediated gentamicin resistance in Staphylococcus aureus encoded by Tn4001. J Med Microbiol 24: 139-144.
18. Holden, M.T., Lindsay, J.A., Corton, C., Quail, M.A., Cockfield, J.D., Pathak, S., etal. (2010) Genome sequence of a recently emerged, highly transmissible, multi-antibiotic- and antiseptic-resistant variant of methicillin-resistant Staphylococcus aureus, sequence type 239 (TW). J Bacteriol 192: 888-892.
19. Kaito, C., Saito, Y., Ikuo, M., Omae, Y., Mao, H., Nagano, G., etal. (2013) Mobile genetic element SCCmec-encoded psm-mec RNA suppresses translation of agrA and attenuates MRSA virulence. PLoS Pathog 9: e1003269.
20. Kennedy, A.D., Bubeck Wardenburg, J., Gardner, D.J., Long, D., Whitney, A.R., Braughton, K.R., etal. (2010) Targeting of alpha-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J Infect Dis 202: 1050-1058.
21. Koskela, A., Nilsdotter-Augustinsson, A., Persson, L., and Soderquist, B. (2009) Prevalence of the ica operon and insertion sequence IS256 among Staphylococcus epidermidis prosthetic joint infection isolates. Eur J Clin Microbiol Infect Dis 28: 655-660.
22. Lanave, C., Preparata, G., Saccone, C., and Serio, G. (1984) A new method for calculating evolutionary substitution rates. J Mol Evol 20: 86-93.
23. Li, D., and Cheung, A. (2008) Repression of hla by rot is dependent on sae in Staphylococcus aureus. Infect Immun 76: 1068-1075.
24. Li, M., Diep, B.A., Villaruz, A.E., Braughton, K.R., Jiang, X., DeLeo, F.R., etal. (2009) Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci USA 106: 5883-5888.
25. Li, M., Cheung, G.Y., Hu, J., Wang, D., Joo, H.S., Deleo, F.R., and Otto, M. (2010) Comparative analysis of virulence and toxin expression of global community-associated methicillin-resistant Staphylococcus aureus strains. J Infect Dis 202: 1866-1876.
26. Limbago, B., Fosheim, G.E., Schoonover, V., Crane, C.E., Nadle, J., Petit, S., etal. (2009) Characterization of methicillin-resistant Staphylococcus aureus isolates collected in 2005 and 2006 from patients with invasive disease: a population-based analysis. J Clin Microbiol 47: 1344-1351.
27. Loessner, I., Dietrich, K., Dittrich, D., Hacker, J., and Ziebuhr, W. (2002) Transposase-dependent formation of circular IS256 derivatives in Staphylococcus epidermidis and Staphylococcus aureus. J Bacteriol 184: 4709-4714.
28. Lyon, B.R., May, J.W., and Skurray, R.A. (1983) Analysis of plasmids in nosocomial strains of multiple-antibiotic-resistant Staphylococcus aureus. Antimicrob Agents Chemother 23: 817-826.
29. Lyon, B.R., Gillespie, M.T., and Skurray, R.A. (1987) Detection and characterization of IS256, an insertion sequence in Staphylococcus aureus. J Gen Microbiol 133: 3031-3038.
30. McEvoy, C.R., Tsuji, B., Gao, W., Seemann, T., Porter, J.L., Doig, K., etal. (2013) Decreased vancomycin susceptibility in Staphylococcus aureus caused by IS256 tempering of WalKR expression. Antimicrob Agents Chemother 57: 3240-3249.
31. McNamara, P.J., and Bayer, A.S. (2005) A rot mutation restores parental virulence to an agr-null Staphylococcus aureus strain in a rabbit model of endocarditis. Infect Immun 73: 3806-3809.
32. McNamara, P.J., Milligan-Monroe, K.C., Khalili, S., and Proctor, R.A. (2000) Identification, cloning, and initial characterization of rot, a locus encoding a regulator of virulence factor expression in Staphylococcus aureus. J Bacteriol 182: 3197-3203.
33. Mahillon, J., and Chandler, M. (1998) Insertion sequences. Microbiol Mol Biol Rev 62: 725-774.
34. Monk, I.R., Shah, I.M., Xu, M., Tan, M.W., and Foster, T.J. (2012) Transforming the untransformable: application of direct transformation to manipulate genetically Staphylococcus aureus and Staphylococcus epidermidis. mBio 3: pii: e00277-11.
35. Nagel, M., Reuter, T., Jansen, A., Szekat, C., and Bierbaum, G. (2011) Influence of ciprofloxacin and vancomycin on mutation rate and transposition of IS256 in Staphylococcus aureus. Int J Med Microbiol 301: 229-236.
36. Novick, R.P., and Geisinger, E. (2008) Quorum sensing in staphylococci. Annu Rev Genet 42: 541-564.
37. Oscarsson, J., Harlos, C., and Arvidson, S. (2005) Regulatory role of proteins binding to the spa (protein A) and sarS (staphylococcal accessory regulator) promoter regions in Staphylococcus aureus NTCC 8325-4. Int J Med Microbiol 295: 253-266.
38. Otto, M. (2013) Community-associated MRSA: what makes them special? Int J Med Microbiol 303: 324-330.
39. Pattengale, N.D., Alipour, M., Bininda-Emonds, O.R., Moret, B.M., and Stamatakis, A. (2010) How many bootstrap replicates are necessary? J Comput Biol 17: 337-354.
40. Peters, P.J., Brooks, J.T., Limbago, B., Lowery, H.K., McAllister, S.K., Mindley, R., etal. (2011) Methicillin-resistant Staphylococcus aureus colonization in HIV-infected outpatients is common and detection is enhanced by groin culture. Epidemiol Infect 139: 998-1008.
41. Pishchany, G., McCoy, A.L., Torres, V.J., Krause, J.C., Crowe, J.E., Jr, Fabry, M.E., and Skaar, E.P. (2010) Specificity for human hemoglobin enhances Staphylococcus aureus infection. Cell Host Microbe 8: 544-550.
42. Roberts, R.B., de Lencastre, A., Eisner, W., Severina, E.P., Shopsin, B., Kreiswirth, B.N., and Tomasz, A. (1998) Molecular epidemiology of methicillin-resistant Staphylococcus aureus in 12 New York hospitals. MRSA Collaborative Study Group. J Infect Dis 178: 164-171.
43. Robinson, D.A., and Enright, M.C. (2004) Evolution of Staphylococcus aureus by large chromosomal replacements. J Bacteriol 186: 1060-1064.
44. Said-Salim, B., Dunman, P.M., McAleese, F.M., Macapagal, D., Murphy, E., McNamara, P.J., etal. (2003) Global regulation of Staphylococcus aureus genes by Rot. J Bacteriol 185: 610-619.
45. Seybold, U., Kourbatova, E.V., Johnson, J.G., Halvosa, S.J., Wang, Y.F., King, M.D., etal. (2006) Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis 42: 647-656.
46. Shopsin, B., Eaton, C., Wasserman, G.A., Mathema, B., Adhikari, R.P., Agolory, S., etal. (2010) Mutations in agr do not persist in natural populations of methicillin-resistant Staphylococcus aureus. J Infect Dis 202: 1593-1599.
47. Simpson, J.T., Wong, K., Jackman, S.D., Schein, J.E., Jones, S.J., and Birol, I. (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19: 1117-1123. doi:10.1101/gr.089532.108
48. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
49. Tenover, F.C., and Goering, R.V. (2009) Methicillin-resistant Staphylococcus aureus strain USA300: origin and epidemiology. J Antimicrob Chemother 64: 441-446.
50. Tenover, F.C., McDougal, L.K., Goering, R.V., Killgore, G., Projan, S.J., Patel, J.B., and Dunman, P.M. (2006) Characterization of a strain of community-associated methicillin-resistant Staphylococcus aureus widely disseminated in the United States. J Clin Microbiol 44: 108-118.
51. Torres, V.J., Attia, A.S., Mason, W.J., Hood, M.I., Corbin, B.D., Beasley, F.C., etal. (2010) Staphylococcus aureus fur regulates the expression of virulence factors that contribute to the pathogenesis of pneumonia. Infect Immun 78: 1618-1628.
52. Uhlemann, A.C., Knox, J., Miller, M., Hafer, C., Vasquez, G., Ryan, M., etal. (2011) The environment as an unrecognized reservoir for community-associated methicillin resistant Staphylococcus aureus USA300: a case-control study. PLoS ONE 6: e22407.
53. Valle, J., Vergara-Irigaray, M., Merino, N., Penades, J.R., and Lasa, I. (2007) sigmaB regulates IS256-mediated Staphylococcus aureus biofilm phenotypic variation. J Bacteriol 189: 2886-2896.
54. Voyich, J.M., Braughton, K.R., Sturdevant, D.E., Whitney, A.R., Said-Salim, B., Porcella, S.F., etal. (2005) Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 175: 3907-3919.
55. Wang, R., Braughton, K.R., Kretschmer, D., Bach, T.H., Queck, S.Y., Li, M., etal. (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13: 1510-1514.
56. Yamamoto, T., Takano, T., Higuchi, W., Iwao, Y., Singur, O., Reva, I., etal. (2012) Comparative genomics and drug resistance of a geographic variant of ST239 methicillin-resistant Staphylococcus aureus emerged in Russia. PLoS ONE 7: e29187.
57. Yang, Z. (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39: 306-314.
58. Yarwood, J.M., Bartels, D.J., Volper, E.M., and Greenberg, E.P. (2004) Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol 186: 1838-1850.
59. Ziebuhr, W., Krimmer, V., Rachid, S., Lossner, I., Gotz, F., and Hacker, J. (1999) A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol Microbiol 32: 345-356.