Evolutionary pathway to increased virulence and epidemic group A Streptococcus disease derived from 3,615 genome sequences

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 17, 2014, Pages

  Nasser, Waleed ^a,b   Beres, Stephen B ^a,b   Olsen, Randall J ^a,b   Dean, Melissa A ^a,b   Rice, Kelsey A ^a,b   Long, S Wesley ^a,b   Kristinsson, Karl G ^b,d   Gottfredsson, Magnus ^c,d   Vuopio, Jaana ^e   Raisanen, Kati ^e   Caugant, Dominique A ^f   Steinbakk, Martin ^f   Low, Donald E ^b,g   McGeer, Allison ^g   Darenberg, Jessica ^h   Henriques Normark, Birgitta ^i,j   Van Beneden, Chris A ^k   Hoffmann, Steen ^l   Musser, James M ^a,b  

^a HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^b HOUSTON METHODIST HOSPITAL   (United States)

^c LANDSPITALI UNIVERSITY HOSPITAL   (Iceland)

^d UNIVERSITY OF ICELAND   (Iceland)

^e UNIVERSITY OF TURKU   (Finland)

^f NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^g MOUNT SINAI HOSPITAL   (Canada)

^h SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

ⁱ KAROLINSKA INSTITUTE   (Sweden)

^j KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^k NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^l STATENS SERUM INSTITUT   (Denmark)

more..

Author keywords

Flesh eating disease; Mobile genetic element; Molecular clock; Pathogenesis; Phylogeography

Indexed keywords

GLYCOSIDASE; HYALURONIC ACID; STREPTOLYSIN O;

ARTICLE; BACTERIAL VIRULENCE; CHROMOSOME; DIVERSIFYING SELECTION; DNA POLYMORPHISM; GENE FREQUENCY; GENE SEQUENCE; GENE TRANSFER; GENETIC DISTANCE; GENOME; GENOMICS; HOST; MOLECULAR INTERACTION; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHARYNGITIS; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROPHAGE; SINGLE NUCLEOTIDE POLYMORPHISM; STEM CELL; STREPTOCOCCUS GROUP A; STREPTOCOCCUS INFECTION;

FLESH-EATING DISEASE; MOBILE GENETIC ELEMENT; MOLECULAR CLOCK; PATHOGENESIS; PHYLOGEOGRAPHY;

ANIMALS; BASE SEQUENCE; DISEASE MODELS, ANIMAL; EPIDEMICS; EVOLUTION, MOLECULAR; FASCIITIS, NECROTIZING; FINLAND; GENES, BACTERIAL; GENOME, BACTERIAL; GENOMICS; HUMANS; INDEL MUTATION; PHARYNGITIS; POLYMORPHISM, SINGLE NUCLEOTIDE; PRIMATES; SELECTION, GENETIC; SEROTYPING; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES; TIME FACTORS; VIRULENCE;

EID: 84899645046     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1403138111     Document Type: Article

References (76)

1. Beall B, Facklam R, Hoenes T, Schwartz B (1997) Survey of emm gene sequences and T-antigen types from systemic Streptococcus pyogenes infection isolates collected in San Francisco, California; Atlanta, Georgia; and Connecticut in 1994 and 1995. J Clin Microbiol 35(5):1231-1235.
2. Bucher A, et al. (1992) Spectrum of disease in bacteraemic patients during a Streptococcus pyogenes serotype M-1 epidemic in Norway in 1988. Eur J Clin Microbiol Infect Dis 11(5):416-426.
3. Carapetis J, Robins-Browne R, Martin D, Shelby-James T, Hogg G (1995) Increasing severity of invasive group A streptococcal disease in Australia: Clinical and molecular epidemiological features and identification of a new virulent M-nontypeable clone. Clin Infect Dis 21(5):1220-1227.
4. Carapetis JR, Steer AC, Mulholland EK, Weber M (2005) The global burden of group A streptococcal diseases. Lancet Infect Dis 5(11):685-694.
5. Chelsom J, Halstensen A, Haga T, Høiby EA (1994) Necrotising fasciitis due to group A streptococci in western Norway: Incidence and clinical features. Lancet 344(8930): 1111-1115.
6. Colman G, Tanna A, Efstratiou A, Gaworzewska ET (1993) The serotypes of Streptococcus pyogenes present in Britain during 1980-1990 and their association with disease. J Med Microbiol 39(3):165-178.
7. Davies HD, et al.; Ontario Group A Streptococcal Study Group (1996) Invasive group A streptococcal infections in Ontario, Canada. N Engl J Med 335(8):547-554.
8. Demers B, et al. (1993) Severe invasive group A streptococcal infections in Ontario, Canada: 1987-1991. Clin Infect Dis 16(6):792-800; discussion 801-792.
9. Gaworzewska E, Colman G (1988) Changes in the pattern of infection caused by Streptococcus pyogenes. Epidemiol Infect 100(2):257-269.
10. Ikebe T, et al.; Working Group for Group A Streptococci in Japan (2003) Changing prevalent T serotypes and emm genotypes of Streptococcus pyogenes isolates from streptococcal toxic shock-like syndrome (TSLS) patients in Japan. Epidemiol Infect 130(3):569-572.
11. Kaul R, McGeer A, Low DE, Green K, Schwartz B (1997) Population-based surveillance for group A streptococcal necrotizing fasciitis: Clinical features, prognostic indicators, and microbiologic analysis of seventy-seven cases. Ontario Group A Streptococcal Study. Am J Med 103(1):18-24.
12. Martin PR, Høiby EA (1990) Streptococcal serogroup A epidemic in Norway 1987-1988. Scand J Infect Dis 22(4):421-429.
13. Muotiala A, Seppälä H, Huovinen P, Vuopio-Varkila J (1997) Molecular comparison of group A streptococci of T1M1 serotype from invasive and noninvasive infections in Finland. J Infect Dis 175(2):392-399.
14. Musser J, Krause R (1998) The revival of group A streptococcal diseases, with a commentary on staphylococcal toxic shock syndrome. Emerging Infections, ed Krause R (Academic Press, New York), pp 185-218.
15. O'Brien KL, et al. (2002) Epidemiology of invasive group a streptococcus disease in the United States, 1995-1999. Clin Infect Dis 35(3):268-276.
16. Schwartz B, Facklam RR, Breiman RF (1990) Changing epidemiology of group A streptococcal infection in the USA. Lancet 336(8724):1167-1171.
17. Sharkawy A, et al.; Ontario Group A Streptococcal Study Group (2002) Severe group a streptococcal soft-tissue infections in Ontario: 1992-1996. Clin Infect Dis 34(4): 454-460.
18. Stevens DL, et al. (1989) Severe group A streptococcal infections associated with a toxic shock-like syndrome and scarlet fever toxin A. N Engl J Med 321(1):1-7.
19. Strömberg A, Romanus V, Burman LG (1991) Outbreak of group A streptococcal bacteremia in Sweden: An epidemiologic and clinical study. J Infect Dis 164(3): 595-598.
20. Tyrrell GJ, et al. (2002) M types of group a streptococcal isolates submitted to the National Centre for Streptococcus (Canada) from 1993 to 1999. J Clin Microbiol 40(12):4466-4471.
21. http://en.wikipedia.org/wiki/Necrotizing-fasciitis. Accessed February 11, 2014.
22. Beres SB, et al. (2002) Genome sequence of a serotype M3 strain of group A Streptococcus: Phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci USA 99(15):10078-10083.
23. Ferretti JJ, et al. (2001) Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci USA 98(8):4658-4663.
24. Sumby P, et al. (2005) Evolutionary origin and emergence of a highly successful clone of serotype M1 group a Streptococcus involved multiple horizontal gene transfer events. J Infect Dis 192(5):771-782.
25. Beres SB, Musser JM (2007) Contribution of exogenous genetic elements to the group A Streptococcus metagenome. PLoS ONE 2(8):e800.
26. Banks DJ, et al. (2004) Progress toward characterization of the group A Streptococcus metagenome: Complete genome sequence of a macrolide-resistant serotype M6 strain. J Infect Dis 190(4):727-738.
27. Fittipaldi N, et al. (2012) Full-genome dissection of an epidemic of severe invasive disease caused by a hypervirulent, recently emerged clone of group A Streptococcus. Am J Pathol 180(4):1522-1534.
28. Green NM, et al. (2005) Genome sequence of a serotype M28 strain of group a streptococcus: Potential new insights into puerperal sepsis and bacterial disease specificity. J Infect Dis 192(5):760-770.
29. Holden MT, et al. (2007) Complete genome of acute rheumatic fever-associated serotype M5 Streptococcus pyogenes strain manfredo. J Bacteriol 189(4):1473-1477.
30. McShan WM, et al. (2008) Genome sequence of a nephritogenic and highly transformable M49 strain of Streptococcus pyogenes. J Bacteriol 190(23):7773-7785.
31. Miyoshi-Akiyama T, Watanabe S, Kirikae T (2012) Complete genome sequence of Streptococcus pyogenes M1 476, isolated from a patient with streptococcal toxic shock syndrome. J Bacteriol 194(19):5466.
32. Smoot JC, et al. (2002) Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc Natl Acad Sci USA 99(7):4668-4673.
33. Zheng PX, et al. (2013) Complete Genome Sequence of emm1 Streptococcus pyogenes A20, a Strain with an Intact Two-Component System, CovRS, Isolated from a Patient with Necrotizing Fasciitis. Genome Announc 1(1).
34. Varaldo PE, Montanari MP, Giovanetti E (2009) Genetic elements responsible for erythromycin resistance in streptococci. Antimicrob Agents Chemother 53(2):343-353.
35. Richter SS, et al. (2005) Macrolide-resistant Streptococcus pyogenes in the United States, 2002-2003. Clin Infect Dis 41(5):599-608.
36. Maamary PG, et al. (2012) Tracing the evolutionary history of the pandemic group A streptococcal M1T1 clone. FASEB J 26(11):4675-4684.
37. Nelson K, Schlievert PM, Selander RK, Musser JM (1991) Characterization and clonal distribution of four alleles of the speA gene encoding pyrogenic exotoxin A (scarlet fever toxin) in Streptococcus pyogenes. J Exp Med 174(5):1271-1274.
38. Grossman D, Cook RG, Sparrow JT, Mollick JA, Rich RR (1990) Dissociation of the stimulatory activities of staphylococcal enterotoxins for T cells and monocytes. J Exp Med 172(6):1831-1841.
39. Kline JB, Collins CM(1996) Analysis of the superantigenic activity of mutant and allelic forms of streptococcal pyrogenic exotoxin A. Infect Immun 64(3):861-869.
40. Musser JM, et al. (1991) Streptococcus pyogenes causing toxic-shock-like syndrome and other invasive diseases: Clonal diversity and pyrogenic exotoxin expression. Proc Natl Acad Sci USA 88(7):2668-2672.
41. Musser JM, et al. (1995) Genetic diversity and relationships among Streptococcus pyogenes strains expressing serotype M1 protein: Recent intercontinental spread of a subclone causing episodes of invasive disease. Infect Immun 63(3):994-1003.
42. Hoe NP, et al. (1999) Rapid selection of complement-inhibiting protein variants in group A Streptococcus epidemic waves. Nat Med 5(8):924-929.
43. Shea PR, et al. (2011) Distinct signatures of diversifying selection revealed by genome analysis of respiratory tract and invasive bacterial populations. Proc Natl Acad Sci USA 108(12):5039-5044.
44. Olsen RJ, Musser JM (2010) Molecular pathogenesis of necrotizing fasciitis. Annu Rev Pathol 5:1-31.
45. Olsen RJ, et al. (2010) Decreased necrotizing fasciitis capacity caused by a single nucleotide mutation that alters a multiple gene virulence axis. Proc Natl Acad Sci USA 107(2):888-893.
46. Virtaneva K, et al. (2005) Longitudinal analysis of the group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc Natl Acad Sci USA 102(25):9014-9019.
47. de Ligt J, et al. (2012) Diagnostic exome sequencing in persons with severe intellectual disability. N Engl J Med 367(20):1921-1929.
48. Abecasis GR, et al.; 1000 Genomes Project Consortium (2012) An integrated map of genetic variation from 1,092 human genomes. Nature 491(7422):56-65.
49. Navin N, et al. (2011) Tumour evolution inferred by single-cell sequencing. Nature 472(7341):90-94.
50. Poznik GD, et al. (2013) Sequencing Y chromosomes resolves discrepancy in time to common ancestor of males versus females. Science 341(6145):562-565.
51. Casali N, et al. (2014) Evolution and transmission of drug-resistant tuberculosis in a Russian population. Nat Genet 46(3):279-286.
52. Chewapreecha C, et al. (2014) Dense genomic sampling identifies highways of pneumococcal recombination. Nat Genet 46(3):305-309.
53. Holt KE, et al. (2013) Tracking the establishment of local endemic populations of an emergent enteric pathogen. Proc Natl Acad Sci USA 110(43):17522-17527.
54. Mather AE, et al. (2013) Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science 341(6153):1514-1517.
55. Zhou Z, et al. (2013) Neutral genomic microevolution of a recently emerged pathogen, Salmonella enterica serovar Agona. PLoS Genet 9(4):e1003471.
56. Aziz RK, et al. (2005) Mosaic prophages with horizontally acquired genes account for the emergence and diversification of the globally disseminated M1T1 clone of Streptococcus pyogenes. J Bacteriol 187(10):3311-3318.
57. Aziz RK, Kotb M (2008) Rise and persistence of global M1T1 clone of Streptococcus pyogenes. Emerg Infect Dis 14(10):1511-1517.
58. Cleary PP, et al. (1992) Clonal basis for resurgence of serious Streptococcus pyogenes disease in the 1980s. Lancet 339(8792):518-521.
59. Cleary PP, LaPenta D, Vessela R, Lam H, Cue D (1998) A globally disseminated M1 subclone of group A streptococci differs from other subclones by 70 kilobases of prophage DNA and capacity for high-frequency intracellular invasion. Infect Immun 66(11):5592-5597.
60. Vlaminckx BJ, et al. (2007) Dynamics in prophage content of invasive and noninvasive M1 and M28 Streptococcus pyogenes isolates in The Netherlands from 1959 to 1996. Infect Immun 75(7):3673-3679.
61. Bricker AL, Carey VJ, Wessels MR (2005) Role of NADase in virulence in experimental invasive group A streptococcal infection. Infect Immun 73(10):6562-6566.
62. Bricker AL, Cywes C, Ashbaugh CD, Wessels MR (2002) NAD+-glycohydrolase acts as an intracellular toxin to enhance the extracellular survival of group A streptococci. Mol Microbiol 44(1):257-269.
63. Chiarot E, et al. (2013) Targeted amino acid substitutions impair streptolysin O toxicity and group A Streptococcus virulence. mBio 4(1):e00387-00312.
64. Limbago B, Penumalli V, Weinrick B, Scott JR (2000) Role of streptolysin O in a mouse model of invasive group A streptococcal disease. Infect Immun 68(11):6384-6390.
65. Madden JC, Ruiz N, Caparon M (2001) Cytolysin-mediated translocation (CMT): A functional equivalent of type III secretion in gram-positive bacteria. Cell 104(1): 143-152.
66. Michos A, et al. (2006) Enhancement of streptolysin O activity and intrinsic cytotoxic effects of the group A streptococcal toxin, NAD-glycohydrolase. J Biol Chem 281(12): 8216-8223.
67. O'Seaghdha M, Wessels MR (2013) Streptolysin O and its co-toxin NAD-glycohydrolase protect group A Streptococcus from Xenophagic killing. PLoS Pathog 9(6):e1003394.
68. Raskova H, Vanecek J (1957) Effects of intraventricular injections of streptolysin O in unanesthetized cats. Science 126(3276):700-701.
69. Riddle DJ, Bessen DE, Caparon MG (2010) Variation in Streptococcus pyogenes NAD+ glycohydrolase is associated with tissue tropism. J Bacteriol 192(14):3735-3746.
70. Sierig G, Cywes C, Wessels MR, Ashbaugh CD (2003) Cytotoxic effects of streptolysin o and streptolysin s enhance the virulence of poorly encapsulated group a streptococci. Infect Immun 71(1):446-455.
71. Stevens DL, Salmi DB, McIndoo ER, Bryant AE (2000) Molecular epidemiology of nga and NAD glycohydrolase/ADP-ribosyltransferase activity among Streptococcus pyogenes causing streptococcal toxic shock syndrome. J Infect Dis 182(4):1117-1128.
72. Tatsuno I, Isaka M, Minami M, Hasegawa T (2010) NADase as a target molecule of in vivo suppression of the toxicity in the invasive M-1 group A Streptococcal isolates. BMC Microbiol 10:144.
73. Timmer AM, et al. (2009) Streptolysin O promotes group A Streptococcus immune evasion by accelerated macrophage apoptosis. J Biol Chem 284(2):862-871.
74. Luca-Harari B, et al.; Strep-EURO Study Group (2009) Clinical and microbiological characteristics of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol 47(4):1155-1165.
75. Shulman ST, et al.; North American Streptococcal Pharyngitis Surveillance Group (2009) Seven-year surveillance of north american pediatric group a streptococcal pharyngitis isolates. Clin Infect Dis 49(1):78-84.
76. Steer AC, Law I, Matatolu L, Beall BW, Carapetis JR (2009) Global emm type distribution of group A streptococci: Systematic review and implications for vaccine development. Lancet Infect Dis 9(10):611-616.