Detection of Streptococcus pyogenes virulence genes in Streptococcus dysgalactiae subsp. equisimilis from Vellore, India
Tóm tắt
Streptococcus dysgalactiae subsp. equisimilis (SDSE), belonging to the group C and G streptococci, are human pathogens reported to cause clinical manifestations similar to infections caused by Streptococcus pyogenes. To scrutinize the distribution of gene coding for S. pyogenes virulence factors in SDSE, 255 isolates were collected from humans infected with SDSE in Vellore, a region in southern India, with high incidence of SDSE infections. Initial evaluation indicated SDSE isolates comprising of 82.35% group G and 17.64% group C. A multiplex PCR system was used to detect 21 gene encoding virulence-associated factors of S. pyogenes, like superantigens, DNases, proteinases, and other immune modulatory toxins. As validated by DNA sequencing of the PCR products, sequences homologous to speC, speG, speH, speI, speL, ssa and smeZ of the family of superantigen coding genes and for DNases like sdaD and sdc were detected in the SDSE collection. Furthermore, there was high abundance (48.12% in group G and 86.6% in group C SDSE) of scpA, the gene coding for C5a peptidase in these isolates. Higher abundance of S. pyogenes virulence factor genes was observed in SDSE of Lancefield group C as compared to group G, even though the incidence rates in former were lower. This study not only substantiates detection of S. pyogenes virulence factor genes in whole genome sequenced SDSE but also makes significant contribution towards the understanding of SDSE and its increasing virulence potential.
Tài liệu tham khảo
Babbar A, Kumar VN, Bergmann R, Barrantes I, Pieper DH, Itzek A, Nitsche-Schmitz DP (2017) Members of a new subgroup of Streptococcus anginosus harbor virulence related genes previously observed in Streptococcus pyogenes. Int J Med Microbiol 307:174–181
Baracco G, Bisno A (2006) Group C and G streptococcal infections: epidemiologic and clinical aspects. In: Fischetti VA, Novick RP, Ferretti JJ (eds) Gram-positive pathogens. American Society for Microbiology, Washington, D.C., pp 222–229
Behera B, Mathur P, Bhardwaj N, Jain N, Misra MC, Kapil A, Singh S (2014) Antibiotic susceptibilities, streptococcal pyrogenic exotoxin gene profiles among clinical isolates of group C or G Streptococcus dysgalactiae subsp. equisimilis & of group G S. anginosus group at a tertiary care centre. Indian J Med Res 139:438–445
Bradley SF, Gordon JJ, Baumgartner DD, Marasco WA, Kauffman CA (1991) Group C streptococcal bacteremia: analysis of 88 cases. Rev Infect Dis 13:270–280
Brahmadathan KN, Koshi G (1989) Importance of group G streptococci in human pyogenic infections. J Trop Med Hyg 92:35–38
Brandt CM, Spellerberg B (2009) Human infections due to Streptococcus dysgalactiae subspecies equisimilis. Clin Infect Dis 49:766–772
Bruun T, Kittang BR, de Hoog BJ, Aardal S, Flaatten HK, Langeland N, Mylvaganam H, Vindenes HA, Skrede S (2013) Necrotizing soft tissue infections caused by Streptococcus pyogenes and Streptococcus dysgalactiae subsp. equisimilis of groups C and G in western Norway. Clin Microbiol Infect 19:E545–E550
Cole JN, Barnett TC, Nizet V, Walker MJ (2011) Molecular insight into invasive group A streptococcal disease. Nat Rev Microbiol 9:724–736
Davies MR, McMillan DJ, Beiko RG et al (2007) Virulence profiling of Streptococcus dysgalactiae subspecies equisimilis isolated from infected humans reveals 2 distinct genetic lineages that do not segregate with their phenotypes or propensity to cause diseases. Clin Infect Dis 44:1442–1454
Efstratiou A (1997) Pyogenic streptococci of Lancefield groups C and G as pathogens in man. J Appl Microbiol 83:72S–79S
Efstratiou A, Lamagni T (2016) Epidemiology of Streptococcus pyogenes. In: Streptococcus pyogenes: basic biology to clinical manifestations
Ferretti JJ, McShan WM, Ajdic D et al (2001) Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci 98:4658–4663
Gherardi G, Imperi M, Palmieri C, Magi G, Facinelli B, Baldassarri L, Pataracchia M, Creti R (2014) Genetic diversity and virulence properties of Streptococcus dysgalactiae subsp. equisimilis from different sources. J Med Microbiol 63:90–98
Gladstone P, Jesudason MV, Sridharan G (2003) Invasive properties of south Indian strains of Streptococcus pyogenes in a HEp-2 cell model. Clin Microbiol Infect 9:1031–1034
Haataja S, Gerlach D (2001) The SpeB virulence factor of Streptococcus pyogenes, a multifunctional secreted and cell surface molecule with strepadhesin, laminin-binding and cysteine protease activity. Mol Microbiol 39:512–519
Haggar A, Nerlich A, Kumar R, Abraham VJ, Brahmadathan KN, Ray P, Dhanda V, Joshua JMJ, Mehra N, Bergmann R, Chhatwal GS, Norrby-Teglund A (2012) Clinical and microbiologic characteristics of invasive Streptococcus pyogenes infections in north and south India. J Clin Microbiol 50:1626–1631
Hashikawa S, Iinuma Y, Ohkura T et al (2004) Characterization of group C and G streptococcal strains that cause streptococcal toxic shock syndrome. J Clin Microbiol 42:186–192
Humar D, Datta V, Bast DJ, Beall B, de Azavedo JCS, Nizet V (2002) Streptolysin S and necrotising infections produced by group G streptococcus. Lancet 359:124–129
Igwe EI, Shewmaker PL, Facklam RR, Farley MM, Beneden C, Beall B (2003) Identification of superantigen genes speM, ssa, and smeZ in invasive strains of beta-hemolytic group C and G streptococci recovered from humans. FEMS Microbiol Lett 229:259–264
Ikebe T, Wada A, Inagaki Y, Sugama K, Suzuki R, Tanaka D, Tamaru A, Fujinaga Y, Abe Y, Shimizu Y, Watanabe H, Working Group for Group A Streptococcus in Japan (2002) Dissemination of the phage-associated novel superantigen gene speL in recent invasive and noninvasive Streptococcus pyogenes M3/T3 isolates in Japan. Infect Immun 70:3227–3233
Kalia A, Bessen DE (2003) Presence of streptococcal pyrogenic exotoxin A and C genes in human isolates of group G streptococci. FEMS Microbiol Lett 219:291–295
Lamagni TL, Darenberg J, Luca-Harari B, Siljander T, Efstratiou A, Henriques-Normark B, Vuopio-Varkila J, Bouvet A, Creti R, Ekelund K, Koliou M, Reinert RR, Stathi A, Strakova L, Ungureanu V, Schalen C, the Strep-EURO Study Group, Jasir A (2008) Epidemiology of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol 46:2359–2367
Luca-Harari B, Darenberg J, Neal S, Siljander T, Strakova L, Tanna A, Creti R, Ekelund K, Koliou M, Tassios PT, van der Linden M, Straut M, Vuopio-Varkila J, Bouvet A, Efstratiou A, Schalen C, Henriques-Normark B, the Strep-EURO Study Group, Jasir A (2009) Clinical and microbiological characteristics of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol 47:1155–1165
Nelson DC, Garbe J, Collin M (2011) Cysteine proteinase SpeB from Streptococcus pyogenes—a potent modifier of immunologically important host and bacterial proteins. Biol Chem 392:1077–1088
Oggioni MR, Pozzi G (1996) A host-vector system for heterologous gene expression in Streptococcus gordonii. Gene 169:85–90
Oster A, Bisno H (2000) Group C and G streptococcal infections: epidemiologic and clinical aspects. In: Gram-positive pathogens. ASM Press, Washington, DC. pp 184–190
Pinho MD, Erol E, Ribeiro-Gonçalves B, Mendes CI, Carriço JA, Matos SC, Preziuso S, Luebke-Becker A, Wieler LH, Melo-Cristino J, Ramirez M (2016) Beta-hemolytic Streptococcus dysgalactiae strains isolated from horses are a genetically distinct population within the Streptococcus dysgalactiae taxon. Sci Rep 6:31736. https://doi.org/10.1038/srep31736
Prabu D, Menon T (2011) Genotypic characterization of toxigenic group C and G streptococci isolated in Chennai, South India. Folia Microbiol (Praha) 56:345–348
Preziuso S, Pinho MD, Attili AR, Melo-Cristino J, Acke E, Midwinter AC, Cuteri V, Ramirez M (2014) PCR based differentiation between Streptococcus dysgalactiae subsp. equisimilis strains isolated from humans and horses. Comp Immunol Microbiol Infect Dis 37:169–172. https://doi.org/10.1016/j.cimid.2014.04.001
Proft T, Webb PD, Handley V, Fraser JD (2003) Two novel superantigens found in both group A and group C Streptococcus. 71:1361–1369
Rato MG, Nerlich A, Bergmann R, Bexiga R, Nunes SF, Vilela CL, Santos-Sanches I, Chhatwal GS (2011) Virulence gene pool detected in bovine group C Streptococcus dysgalactiae subsp. dysgalactiae isolates by use of a group A S. pyogenes virulence microarray. J Clin Microbiol 49:2470–2479
Reissmann S, Friedrichs C, Rajkumari R et al (2010) Contribution of Streptococcus anginosus to infections caused by groups C and G streptococci, southern India. Emerg Infect Dis 16:656–663
Sachse S, Seidel P, Gerlach D et al (2002) Superantigen-like gene(s) in human pathogenic Streptococcus dysgalactiae, subsp. equisimilis: genomic localisation of the gene encoding streptococcal pyrogenic exotoxin G (speGdys). FEMS Immunol Med Microbiol 34:159–167
Traverso F, Blanco A, Villalón P et al (2017) Molecular characterization of invasive Streptococcus dysgalactiae subsp. equisimilis. Multicenter study: Argentina 2011–2012. Rev Argent Microbiol 48:279–289
Tsai CT, Chi CY, Ho CM, Lin PC, Chou CH, Wang JH, Wang JH, Lin HC, Tien N, Lin KH, Ho MW, Lu JJ (2014) Correlation of virulence genes to clinical manifestations and outcome in patients with Streptococcus dysgalactiae subspecies equisimilis bacteremia. J Microbiol Immunol Infect 47:462–468
Watanabe S, Takemoto N, Ogura K, Miyoshi-Akiyama T (2016) Severe invasive streptococcal infection by Streptococcus pyogenes and Streptococcus dysgalactiae subsp. equisimilis. Microbiol Immunol 60:1–9
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703