Abstract
Streptococcus pyogenes is a species of Gram-positive bacteria. It is also known as Group A Streptococcus (GAS) that causes pathogenesis to humans only. The GAS infection has several manifestations including invasive illness. Current research has linked the molecular modes of GAS virulence with substantial sequencing determinations for the isolation of genomes. These advances help to comprehend the molecular evolution resulting in the pandemic strains. Thus, it is indispensable to reconsider the philosophy that involves GAS pathogenesis. The recent investigations involve studying GAS in the nasopharynx and its capability to cause infection or asymptomatically reside in the host. These advances have been discussed in this article with an emphasis on the natural history of GAS and the evolutionary change in the pandemic strains. In addition, this review describes the unique functions for major pathogenicity determinants to comprehend their physiological effects.
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References
Abel S, Abel zur Wiesch P, Davis BM, Waldor MK (2015) Analysis of bottlenecks in experimental models of infection. PLoS Pathog 11:e1004823
Alam FM, Bateman C, Turner CE, Wiles S, Sriskandan S (2013a) Non-invasive monitoring of Streptococcus pyogenes vaccine efficacy using biophotonic imaging. PLoS ONE 8:e82123
Alam FM, Turner CE, Smith K, Wiles S, Sriskandan S (2013b) Inactivation of the CovR/S virulence regulator impairs infection in an improved murine model of Streptococcus pyogenes naso-pharyngeal infection. PLoS ONE 8:e61655
Andersen BR, Van Epps DE (1972) Suppression of chemotatic activity of human neutrophils by streptolysin O. J Infect Dis 125:353–359
Andreoni F, Ogawa T, Ogawa M, Madon J, Uchiyama S, Schuepbach RA, Zinkernagel AS (2014) The IL-8 protease SpyCEP is detrimental for Group A Streptococcus host-cells interaction and biofilm formation. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00339
Aziz R, Kotb M (2008) Rise and persistence of global M1T1 clone of Streptococcus pyogenes. Emerg Infect Dis 14:1511–1517
Babbar A, Barrantes I, Pieper DH, Itzek A (2019) Superantigen SpeA attenuates the biofilm forming capacity of Streptococcus pyogenes. J Microbiol 57(7):626–636
Bao YJJ, Liang Z, Mayfield JA, Lee SW, Ploplis VA, Castellino FJ (2015) CovRS regulated transcriptome analysis of a hypervirulent M23 strain of Group A Streptococcus pyogenes provides new insights on virulence determinants. J Bacteriol 197:3191–3205
Bastiat-Sempe B, Love JF, Lomayesva N, Wessels MR (2014) Streptolysin O and NAD-glycohydrolase prevent phagolysosome acidification and promote Group A Streptococcus survival in macrophages. mBio 5:e01690–e1714
Beres S, Kachroo P, Nasser W, Olsen RJ, Zhu L, Flores AR, de la Riva I, Paez-Mayorga J, Jimenez FE, Cantu C, Vuopio J, Jalava J, Kristinsson KG, Gottfredsson M, Corander J, Fittipaldi N, Di Luca MC, Petrelli D, Vitali LA, Raiford A, Jenkins L, Musser JM (2016) Transcriptome remodeling contributes to epidemic disease caused by the human pathogen Streptococcus pyogenes. MBio 7:e00403–e416
Bessen D (2009) Population biology of the human restricted pathogen, Streptococcus pyogenes. Infect Genet Evol 9:581–593
Bragonzi A, Paroni M, Nonis A, Cramer N, Montanari S, Rejman J, Di Serio C, Döring G, Tümmler B (2009) Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am J Resp Crit Care 180:138–145
Brown SP, Cornforth DM, Mideo N (2012) Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends Microbiol 20:336–342
Buckley SJ, Timms P, Davies MR, McMillan DJ (2018) In silico characterisation of the two-component system regulators of Streptococcus pyogenes. PLoS ONE 13(6):e0199163. https://doi.org/10.1371/journal.pone.0199163
Carapetis JR, Steer AC, Mulholland EK, Weber M (2005) The global burden of group A streptococcal diseases. Lancet Infect Dis 5:685–694
Chandrasekaran S, Caparon MG (2015) The Streptococcus pyogenes NAD(+) glycohydrolase modulates epithelial cell PARylation and HMGB1 release. Cell Microbiol 17:1376–1390
Churchward G (2007) The two faces of Janus: virulence gene regulation by CovR/S in group A streptococci. Mol Microbiol 64:34–41
Cole JN, Pence MA, von Köckritz-Blickwede M, Hollands A, Gallo RL, Walker MJ, Nizet V (2010) M protein and hyaluronic acid capsule are essential for in vivo selection of covRS mutations characteristic of invasive serotype M1T1 Group A Streptococcus. mBio 1:e00191–e210
Cole JN, Barnett TC, Nizet V, Walker MJ (2011) Molecular insight into invasive group A streptococcal disease. Nat Rev Microbiol 9:724–736
Commons R, Smeesters PR, Proft T, Fraser JD, Robins-Browne R, Curtis N (2014) Streptococcal superantigens: categorization and clinical associations. Trends Mol Med 20:48–62
Cywes C, Stamenkovic I, Wessels MR (2000) CD44 as a receptor for colonization of the pharynx by Group A Streptococcus. J Clin Invest 106:995–1002
Das S, Lindemann C, Young BC, Muller J, Österreich B, Ternette N, Winkler AC, Paprotka K, Reinhardt R, Förstner KU, Allen E, Flaxman A, Yamaguchi Y, Rollier CS, van Diemen P, Blättner S, Remmele CW, Selle M, Dittrich M, Müller T, Vogel J, Ohlsen K, Crook DW, Massey R, Wilson DJ, Rudel T, Wyllie DH, Fraunholz MJ (2016) Natural mutations in a Staphylococcus aureus virulence regulator attenuate cytotoxicity but permit bacteremia and abscess formation. Proc Natl Acad Sci USA 113:E3101–E3110
DeMuri GP, Wald ER (2014) The group A streptococcal carrier state reviewed: still an enigma. J Pediatr Infect Dis Soc 3:336–342
Deng L, Spencer BL, Holmes JA, Mu R, Rego S, Weston TA, Hu Y, Sanches GF, Yoon S, Park N, Nagao PE, Jenkinson HF, Thornton JA, Seo KS, Nobbs AH, Doran KS (2019) The Group B Streptococcal surface antigen I/II protein, BspC, interacts with host Vimentin to promote adherence to brain endothelium and inflammation during the pathogenesis of meningitis. PLoS Pathog 15(6):e1007848
Engleberg NC, Heath A, Miller A, Rivera C, DiRita VJ (2001) Spontaneous mutations in the CsrRS two-component regulatory system of Streptococcus pyogenes result in enhanced virulence in a murine model of skin and soft tissue infection. J Infect Dis 183:1043–1054
Federle MJ, McIver KS, Scott JR (1999) A response regulator that represses transcription of several virulence operons in the Group A Streptococcus. J Bacteriol 181:3649–3657
Feng W, Liu M, Chen DG, Yiu R, Fang FC, Lei B (2016) Contemporary pharyngeal and invasive emm1 and invasive emm12 Group A Streptococcus isolates exhibit similar in vivo selection for CovRS mutants in mice. PLoS ONE 11:e0162742
Flores AR, Jewell BE, Olsen RJ, Shelburne SA, Fittipaldi N, Beres SB, Musser JM (2014) Asymptomatic carriage of Group A Streptococcus is associated with elimination of capsule production. Infect Immun 82:3958–3967
Friães A, Pato C, Melo-Cristino J, Ramirez M (2015) Consequences of the variability of the CovRS and RopB regulators among Streptococcus pyogenes causing human infections. Sci Rep. https://doi.org/10.1038/srep12057
Gaworzewska K, Colman M (1988) Changes in the pattern of infection caused by Streptococcus pyogenes. Epidemiol Infect 100:257–269
Gellatly SL, Hancock RE (2013) Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis 67:159–173
Gergova R, Muhtarova A, Mitov I, Setchanova L, Mihova K, Kaneva R, Markovska R (2019) Relation between emm types and virulence gene profiles among Bulgarian Streptococcus pyogenes clinical isolates. Infect Dis (Lond) 51(9):668–675
Gogos A, Federle MJ (2019) Modeling Streptococcus pyogenes pharyngeal colonization in the mouse. Front Cell Infect Microbiol 2(9):137
Graham MR, Smoot LM, Migliaccio CA, Virtaneva K, Sturdevant DE, Porcella SF, Federle MJ, Adams GJ, Scott JR, Musser JM (2002) Virulence control in Group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling. Proc Natl Acad Sci USA 99:13855–13860
Happonen L, Hauri S, Svensson Birkedal G, Karlsson C, de Neergaard T, Khakzad H, Nordenfelt P, Wikström M, Wisniewska M, Björck L, Malmström L, Malmström J (2019) A quantitative Streptococcus pyogenes-human protein-protein interaction map reveals localization of opsonizing antibodies. Nat Commun 10(1):2727
Heath A, DiRita VJ, Barg NL, Engleberg NC (1999) A two-component regulatory system, CsrR-CsrS, represses expression of three Streptococcus pyogenes virulence factors, hyaluronic acid capsule, streptolysin S, and pyrogenic exotoxin B. Infect Immun 67:5298–5305
Hollands A, Pence MA, Timmer AM, Osvath SR, Turnbull L, Whitchurch CB, Walker MJ, Nizet V (2010) Genetic switch to hypervirulence reduces colonization phenotypes of the globally disseminated Group A Streptococcus M1T1 clone. J Infect Dis 202:11–19
Ikebe T, Ato M, Matsumura T, Hasegawa H, Sata T, Kobayashi K, Watanabe H (2010) Highly frequent mutations in negative regulators of multiple virulence genes in group A streptococcal toxic shock syndrome isolates. PLoS Pathog 6:e1000832
Iovino F, Hammarlöf DL, Garriss G, Brovall S, Nannapaneni P, Henriques-Normark B (2016) Pneumococcal meningitis is promoted by single cocci expressing pilus adhesin RrgA. J Clin Invest 126:2821–2826
Kansal RG, McGeer A, Low DE, Norrby-Teglund A, Kotb M (2000) Inverse relation between disease severity and expression of the streptococcal cysteine protease, SpeB, among clonal M1T1 isolates recovered from invasive group A streptococcal infection cases. Infect Immun 68:6362–6369
Kasper K, Zeppa JJ, Wakabayashi AT, Xu SX, Mazzuca DM, Welch I, Baroja ML, Kotb M, Cairns E, Cleary PP, Haeryfar SM, McCormick JK (2014) Bacterial superantigens promote acute nasopharyngeal infection by Streptococcus pyogenes in a human MHC class II-dependent manner. PLoS Pathog 10:e1004155
Kline JB, Collins CM (1996) Analysis of the superantigenic activity of mutant and allelic forms of streptococcal pyrogenic exotoxin A. Infect Immun 64:861–869
Kono M, Zafar MA, Zuniga M, Roche AM, Hamaguchi S, Weiser JN (2016) Single cell bottlenecks in the pathogenesis of Streptococcus pneumoniae. PLoS Pathog 12:e1005887
Laabei M, Uhlemann AC, Lowy FD, Austin ED, Yokoyama M, Ouadi K, Feil E, Thorpe HA, Williams B, Perkins M, Peacock SJ, Clarke SR, Dordel J, Holden M, Votintseva AA, Bowden R, Crook DW, Young BC, Wilson DJ, Recker M, Massey RC (2015) Evolutionary trade-offs underlie the multifaceted virulence of Staphylococcus aureus. PLoS Biol 13:e1002229
Latronico F, Nasser W, Puhakainen K, Ollgren J, Hyyryläinen HL, Beres SB, Lyytikäinen O, Jalava J, Musser JM, Vuopio J (2016) Genomic characteristics behind spread of bacteremic Group A Streptococcus type emm89 in Finland, 2004–2014. J Infect Dis 214:1987–1995
Le Rhun A, Escalera-Maurer A, Bratovič M, Charpentier E (2019) CRISPR-Cas in Streptococcus pyogenes. RNA Biol 16(4):380–389
Lefébure T, Richards VP, Lang P, Pavinski-Bitar P, Stanhope MJ (2012) Gene repertoire evolution of Streptococcus pyogenes inferred from phylogenomic analysis with Streptococcus canis and Streptococcus dysgalactiae. PLoS ONE 7:e37607
Li Y, Thompson CM, Trzciński K, Lipsitch M (2013) Within host selection is limited by effective population of Streptococcus pneumoniae during nasopharyngeal colonization. Infect Immun 82:1579–1590
Li J, Liu G, Feng W, Zhou Y, Liu M, Wiley JA, Lei B (2014) Neutrophils select hypervirulent CovRs mutants of M1T1 Group A Streptococcus during subcutaneous infection of mice. Infect Immun 82:4534–4543
Lin JN, Chang LL, Lai CH, Lin HH, Chen YH (2014) Association between polymorphisms in the csrRS two-component regulatory system and invasive group A streptococcal infection. Eur J Clin Microbiol Infect Dis 33:735–743
Liu G, Feng W, Li D, Liu M, Nelson DC, Lei B (2015) The Mga regulon but not deoxyribonuclease Sda1 of invasive M1T1 Group A Streptococcus contributes to in vivo selection of CovRS mutations and resistance to innate immune killing mechanisms. Infect Immun 83:4293–4303
Logsdon L, Håkansson AP, Cortés G, Wessels MR (2011) Streptolysin O inhibits clathrin-dependent internalization of Group A Streptococcus. MBio 15(2):e00332–e410
Lorè N, Cigana C, De Fino I, Riva C, Juhas M, Schwager S, Eberl L, Bragonzi A (2012) Cystic fibrosis-niche adaptation of Pseudomonas aeruginosa reduces virulence in multiple infection hosts. PLoS ONE 7:e35648
Lynskey N, Goulding D, Gierula M, Turner CE, Dougan G, Edwards RJ, Sriskandan S (2013) RocA truncation underpins hyper-encapsulation, carriage longevity and transmissibility of serotype M18 group A streptococci. PLoS Pathog 9:e1003842
Lysenko E, Lijek RS, Brown SP, Weiser JN (2009) Within-host competition drives selection for the capsule virulence determinant of Streptococcus pneumoniae. Curr Biol 20:1222–1226
Maamary P, Ben Zakour NL, Cole JN, Hollands A, Aziz RK, Barnett TC, Cork AJ, Henningham A, Sanderson-Smith M, McArthur JD, Venturini C, Gillen CM, Kirk JK, Johnson DR, Taylor WL, Kaplan EL, Kotb M, Nizet V, Beatson SA, Walker MJ (2012) Tracing the evolutionary history of the pandemic group A streptococcal M1T1 clone. FASEB J 26:4675–4684
Martin J (2016) The Streptococcus pyogenes carrier state. In: Ferretti JJ, Stevens DL, Fischetti VA (eds) Streptococcus pyogenes: basic biology to clinical manifestations. University of Oklahoma Health Sciences Center, Oklahoma City, pp 587–600
Mashburn-Warren L, Morrison DA (2012) The cryptic competence pathway in Streptococcus pyogenes is controlled by a peptide pheromone. J Bacteriol 194:4589–4600
Mayfield JA, Liang Z, Agrahari G, Lee SW, Donahue DL, Ploplis VA, Castellino FJ (2014) Mutations in the control of virulence sensor gene from Streptococcus pyogenes after infection in mice lead to clonal bacterial variants with altered gene regulatory activity and virulence. PLoS ONE 9:e100698
McMillan DJ, Beiko RG, Geffers R, Buer J, Schouls LM, Vlaminckx BJ, Wannet WJ, Sriprakash KS, Chhatwal GS (2006) Genes for the majority of group A streptococcal virulence factors and extracellular surface proteins do not confer an increased propensity to cause invasive disease. Clin Infect Dis 43:884–891
Nasser W, Beres SB, Olsen RJ, Dean MA, Rice KA, Long SW, Kristinsson KG, Gottfredsson M, Vuopio J, Raisanen K, Caugant DA, Steinbakk M, Low DE, McGeer A, Darenberg J, Henriques-Normark B, Van Beneden CA, Hoffmann S, Musser JM (2014) Evolutionary pathway to increased virulence and epidemic Group A Streptococcus disease derived from 3,615 genome sequences. Proc Natl Acad Sci USA 111:E1768–E1776
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 174:1271–1274
Nelson AL, Roche AM, Gould JM, Chim K, Ratner AJ, Weiser JN (2007) Capsule enhances pneumococcal colonization by limiting mucus-mediated clearance. Infect Immun 75:83–90
Nitzsche R, Rosenheinrich M, Kreikemeyer B, Oehmcke-Hecht S (2015) Streptococcus pyogenes triggers activation of the human contact system by streptokinase. Infect Immun 83:3035–3042
Nye TM, Jacob KM, Holley EK, Nevarez JM, Dawid S, Simmons LA, Watson ME Jr (2019) DNA methylation from a Type I restriction modification system influences gene expression and virulence in Streptococcus pyogenes. PLoS Pathog 15(6):e1007841
O’Neill AM, Thurston TL, Holden DW (2016) Cytosolic replication of Group A Streptococcus in human macrophages. mBio 7:e00020–e116
O’Seaghdha M, Wessels M (2013) Streptolysin O and its co-toxin NAD-glycohydrolase protect Group A Streptococcus from xenophagic killing. PLoS Pathog 9:e1003394
Olsen RJ, Raghuram A, Cantu C, Hartman MH, Jimenez FE, Lee S, Ngo A, Rice KA, Saddington D, Spillman H, Valson C, Flores AR, Beres SB, Long SW, Nasser W, Musser JM (2015) The majority of 9,729 Group A Streptococcus strains causing disease secrete SpeB cysteine protease: pathogenesis implications. Infect Immun 83:4750–4758
Pato C, Melo-Cristino J, Ramirez M, Friães A (2018) Streptococcus pyogenes causing skin and soft tissue infections are enriched in the recently emerged emm89 clade 3 and are not associated with abrogation of CovRS. Front Microbiol 9:2372
Pezzulo A, Gutiérrez J, Duschner KS, McConnell KS, Taft PJ, Ernst SE, Yahr TL, Rahmouni K, Klesney-Tait J, Stoltz DA, Zabner J (2011) Glucose depletion in the airway surface liquid Is essential for sterility of the airways. PLoS ONE 6:e16166
Philips B, Meguer JX, Redman J, Baker EH (2003) Factors determining the appearance of glucose in upper and lower respiratory tract secretions. Intens Care Med 29:2204–2210
Proft T, Fraser JD (2016) Streptococcal superantigens: biological properties and potential role in disease. In: Ferretti JJ, Stevens DL, Fischetti VA (eds) Streptococcus pyogenes: basic biology to clinical manifestations. University of Oklahoma Health Sciences Center, Oklahoma City, pp 445–486
Rogers S, Commons R, Danchin MH, Selvaraj G, Kelpie L, Curtis N, Robins-Browne R, Carapetis JR (2007) Strain prevalence, rather than innate virulence potential, is the major factor responsible for an increase in serious Group A Streptococcus infections. J Infect Dis 195:1625–1633
Rosinski-Chupin I, Sauvage E, Fouet A, Poyart C, Glaser P (2019) Conserved and specific features of Streptococcus pyogenes and Streptococcusagalactiae transcriptional landscapes. BMC Genomics 20(1):236
Schrager HM, Albertí S, Cywes C, Dougherty GJ, Wessels MR (1998) Hyaluronic acid capsule modulates M protein-mediated adherence and acts as a ligand for attachment of Group A Streptococcus to CD44 on human keratinocytes. J Clin Invest 101:1708–1716
Shumba P, Mairpady Shambat S, Siemens N (2019) The role of streptococcal and staphylococcal exotoxins and proteases in human necrotizing soft tissue infections. Toxins (Basel) 11(6):E332
Siegel SJ, Weiser JN (2015) Mechanisms of bacterial colonization of the respiratory tract. Annu Rev Microbiol 69:425–444
Smoot JC, Korgenski EK, Daly JA, Veasy LG, Musser JM (2002) Molecular analysis of Group A Streptococcus type emm18 isolates temporally associated with acute rheumatic fever outbreaks in Salt Lake City, Utah. J Clin Microbiol 40:1805–1810
Steer A, 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 9:611–616
Stevens DL, Bryant AE (2016) Severe group A streptococcal infections. In: Ferretti JJ, Stevens DL, Fischetti VA (eds) Streptococcus pyogenes: basic biology to clinical manifestations. University of Oklahoma Health Sciences Center, Oklahoma City, pp 741–770
Sumby P, Whitney AR, Graviss EA, DeLeo FR, Musser JM (2006) Genome-wide analysis of group a streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog 2:e5
Treviño J, Perez N, Ramirez-Peña E, Liu Z, Shelburne SA 3rd, Musser JM, Sumby P (2009) CovS simultaneously activates and inhibits the CovR-mediated repression of distinct subsets of Group A Streptococcus virulence factor-encoding genes. Infect Immun 77:3141–3149
Turner CE, Abbott J, Lamagni T, Holden MT, David S, Jones MD, Game L, Efstratiou A, Sriskandan S (2015) Emergence of a new highly successful acapsular Group A Streptococcus clade of genotype emm89 in the United Kingdom. mBio 6:e00622–e715
Uchiyama S, Döhrmann S, Timmer AM, Dixit N, Ghochani M, Bhandari T, Timmer JC, Sprague K, Bubeck-Wardenburg J, Simon SI, Nizet V (2015) Streptolysin O rapidly impairs neutrophil oxidative burst and antibacterial responses to Group A Streptococcus. Front Immunol. https://doi.org/10.3389/fim-mu.2015.00581
Van Opijnen T, Camilli A (2012) A fine scale phenotype–genotype virulence map of a bacterial pathogen. Genome Res 22:2541–2551
Virtaneva K, Porcella SF, Graham MR, Ireland RM, Johnson CA, Ricklefs SM, Babar I, Parkins LD, Romero RA, Corn GJ, Gardner DJ, Bailey JR, Parnell MJ, Musser JM (2005) Longitudinal analysis of the Group A Streptococcus transcriptome in experimental pharyngitis in cynomolgus macaques. Proc Natl Acad Sci USA 102:9014–9019
Waldetoft K, Mohanty T, Karlsson C, Mörgelin M, Frick IM, Malmström J, Björck L (2016) Saliva-induced clotting captures streptococci: novel roles for coagulation and fibrinolysis in host defense and immune evasion. Infect Immun 84:2813–2823
Walker MJ, Hollands A, Sanderson-Smith ML, Cole JN, Kirk JK, Henningham A, McArthur JD, Dinkla K, Aziz RK, Kansal RG, Simpson AJ, Buchanan JT, Chhatwal GS, Kotb M, Nizet V (2007) DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat Med 13:981–985
Watson ME, Nielsen HV, Hultgren SJ, Caparon MG (2013) Murine vaginal colonization model for investigating asymptomatic mucosal carriage of Streptococcus pyogenes. Infect Immun 81:1606–1617
Watson ME, Neely MN, Caparon MG (2016) Animal models of Streptococcus pyogenes infection. In: Ferretti JJ, Stevens DL, Fischetti VA (eds) Streptococcus pyogenes: basic biology to clinical manifestations. University of Oklahoma Health Sciences Center, Oklahoma City, pp 629–660
Weckel A, Ahamada D, Bellais S, Méhats C, Plainvert C, Longo M, Poyart C, Fouet A (2018) The N-terminal domain of the R28 protein promotes emm28 Group A Streptococcus adhesion to host cells via direct binding to three integrins. J Biol Chem 293(41):16006–16018
Wollein Waldetoft K, Råberg L (2014) To harm or not to harm? On the evolution and expression of virulence in group A streptococci. Trends Microbiol 22:7–13
Young B, Golubchik T, Batty EM, Fung R, Larner-Svensson H, Votintseva AA, Miller RR, Godwin H, Knox K, Everitt RG, Iqbal Z, Rimmer AJ, Cule M, Ip CL, Didelot X, Harding RM, Donnelly P, Peto TE, Crook DW, Bowden R, Wilson DJ (2012) Evolutionary dynamics of Staphylococcus aureus during progression from carriage to disease. Proc Natl Acad Sci USA 109:4550–4555
Zhu L, Olsen RJ, Nasser W, Morales IR, Musser JM (2015a) Trading capsule for increased cytotoxin production: contribution to virulence of a newly emerged clade of emm89 Streptococcus pyogenes. mBio 6:01378–1415
Zhu L, Olsen RJ, Nasser W, Beres SB, Vuopio J, Kristinsson KG, Gottfredsson M, Porter AR, DeLeo FR, Musser JM (2015b) A molecular trigger for intercontinental epidemics of Group A Streptococcus. J Clin Invest 125:3545–3559
Zhu L, Olsen RJ, Beres SB, Eraso JM, Saavedra MO, Kubiak SL, Cantu CC, Jenkins L, Charbonneau ARL, Waller AS, Musser JM (2019) Gene fitness landscape of Group A Streptococcus during necrotizing myositis. J Clin Invest 129(2):887–901
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Ijaz, M., Ameen, F., Alfoteih, Y.A. et al. Dissecting Streptococcus pyogenes interaction with human. Arch Microbiol 202, 2023–2032 (2020). https://doi.org/10.1007/s00203-020-01932-w
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DOI: https://doi.org/10.1007/s00203-020-01932-w