1887

Abstract

In some species, the population structure of pathogenic bacteria is clonal. However, the mechanisms that determine the predominance and persistence of specific bacterial lineages of group C remain poorly understood. In Brazil, a previous study revealed the predominance of two main lineages of subsp. (SDSE).

The aim of this study was to assess the virulence and fitness advantages that might explain the predominance of these SDSE lineages for a long period of time.

typing was determined by DNA sequencing. Adhesion and invasion tests were performed using human bronchial epithelial cells (16HBE14o-). Biofilm formation was tested on glass surfaces and the presence of virulence genes was assessed by PCR. Additionally, virulence was studied using models and competitive fitness was analysed in murine models.

The predominant lineages A and B were mostly typed as 839 and 6979, respectively. Notably, these lineages exhibited a superior ability to adhere and invade airway cells. Furthermore, the dominant lineages were more prone to induce aversive olfactory learning and more likely to kill . In the competitive fitness assays, they also showed increased adaptability. Consistent with the increased virulence observed in the and models, the predominant lineages A and B showed a higher number of virulence-associated genes and a superior ability to accumulate biofilm.

These results suggest strongly that this predominance did not occur randomly but rather was due to adaptive mechanisms that culminated in increased colonization and other bacterial properties that might confer increased bacteria–host adaptability to cause disease.

Funding
This study was supported by the:
  • Agnes Marie Sá Figueiredo , Conselho Nacional de Desenvolvimento Científico e Tecnológico , (Award 303067/2015-2)
  • Agnes Marie Sá Figueiredo , Coordenação de Aperfeiçoamento de Pessoal de Nível Superior , (Award Finance code 001)
  • Agnes Marie Sá Figueiredo , Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro , (Award E-26/010001764/2014 and E-26/202.603/2017)
  • Agnes Marie Sá Figueiredo , Conselho Nacional de Desenvolvimento Científico e Tecnológico , (Award 303067/2015-2)
  • Agnes Marie Sá Figueiredo , Coordenação de Aperfeiçoamento de Pessoal de Nível Superior , (Award Finance code 001)
  • Agnes Marie Sá Figueiredo , Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro , (Award E-26/010001764/2014 and E-26/202.603/2017)
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2020-03-03
2020-06-04
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References

  1. Sunaoshi K, Murayama SY, Adachi K, Yagoshi M, Okuzumi K et al. Molecular emm genotyping and antibiotic susceptibility of Streptococcus dysgalactiae subsp. equisimilis isolated from invasive and non-invasive infections. J Med Microbiol 2010; 59:82–88 [CrossRef][PubMed]
    [Google Scholar]
  2. Brandt CM, Spellerberg B. Human infections due to Streptococcus dysgalactiae subspecies equisimilis . Clin Infect Dis 2009; 49:766–772 [CrossRef][PubMed]
    [Google Scholar]
  3. Haidan A, Talay SR, Rohde M, Sriprakash KS, Currie BJ et al. Pharyngeal carriage of group C and group G streptococci and acute rheumatic fever in an Aboriginal population. Lancet 2000; 356:1167–1169 [CrossRef][PubMed]
    [Google Scholar]
  4. Izumi M, Hiraiwa T, Tomioka H, Komura M, Hayashi Y. Fatal necrotizing myositis from fulminant Streptococcus dysgalactiae subspecies equisimilis (SDSE) infection: A case report of autopsy images. J Gen Fam Med 2018; 19:50–52 [CrossRef][PubMed]
    [Google Scholar]
  5. Rantala S, Vähäkuopus S, Vuopio-Varkila J, Vuento R, Syrjänen J. Streptococcus dysgalactiae subsp. equisimilis bacteremia, Finland, 1995–2004. Emerg Infect Dis 2010; 16:843–846 [CrossRef][PubMed]
    [Google Scholar]
  6. Takahashi T, Ubukata K, Watanabe H. Invasive infection caused by Streptococcus dysgalactiae subsp. equisimilis: characteristics of strains and clinical features. J Infect Chemother 2011; 17:1–10 [CrossRef][PubMed]
    [Google Scholar]
  7. Rantala S. Streptococcus dysgalactiae subsp. equisimilis bacteremia: an emerging infection. Eur J Clin Microbiol Infect Dis 2014; 33:1303–1310 [CrossRef][PubMed]
    [Google Scholar]
  8. Laus F, Preziuso S, Spaterna A, Beribè F, Tesei B et al. Clinical and epidemiological investigation of chronic upper respiratory diseases caused by beta-haemolytic Streptococci in horses. Comp Immunol Microbiol Infect Dis 2007; 30:247–260 [CrossRef][PubMed]
    [Google Scholar]
  9. Silva LG, Genteluci GL, Corrêa de Mattos M, Glatthardt T, Sá Figueiredo AM et al. Group C Streptococcus dysgalactiae subsp. equisimilis in south-east Brazil: genetic diversity, resistance profile and the first report of human and equine isolates belonging to the same multilocus sequence typing lineage. J Med Microbiol 2015; 64:551–558 [CrossRef][PubMed]
    [Google Scholar]
  10. Abdelsalam M, Chen S-C, Yoshida T. Dissemination of streptococcal pyrogenic exotoxin G (spegg) with an IS-like element in fish isolates of Streptococcus dysgalactiae . FEMS Microbiol Lett 2010; 309:no–113 [CrossRef][PubMed]
    [Google Scholar]
  11. Babbar A, Itzek A, Pieper DH, Nitsche-Schmitz DP. Detection of Streptococcus pyogenes virulence genes in Streptococcus dysgalactiae subsp. equisimilis from Vellore, India. Folia Microbiol 2018; 63:581–586 [CrossRef][PubMed]
    [Google Scholar]
  12. Gherardi G, Imperi M, Palmieri C, Magi G, Facinelli B et al. Genetic diversity and virulence properties of Streptococcus dysgalactiae subsp. equisimilis from different sources. J Med Microbiol 2014; 63:90–98 [CrossRef][PubMed]
    [Google Scholar]
  13. Nobbs AH, Lamont RJ, Jenkinson HF. Streptococcus adherence and colonization. Microbiol Mol Biol Rev 2009; 73:407–450 [CrossRef][PubMed]
    [Google Scholar]
  14. Sachse S, Seidel P, Gerlach D, Günther E, Rödel J et al. Superantigen-like gene(s) in human pathogenic Streptococcus dysgalactiae, subsp equisimilis: genomic localisation of the gene encoding streptococcal pyrogenic exotoxin G (speG(dys)). FEMS Immunol Med Microbiol 2002; 34:159–167 [CrossRef][PubMed]
    [Google Scholar]
  15. Fischetti VA. Streptococcal M protein: molecular design and biological behavior. Clin Microbiol Rev 1989; 2:285–314 [CrossRef][PubMed]
    [Google Scholar]
  16. Shimomura Y, Okumura K, Murayama SY, Yagi J, Ubukata K et al. Complete genome sequencing and analysis of a Lancefield group G Streptococcus dysgalactiae subsp. equisimilis strain causing streptococcal toxic shock syndrome (STSS). BMC Genomics 2011; 12:17 [CrossRef][PubMed]
    [Google Scholar]
  17. Horii T, Izumida S, Takeuchi K, Tada T, Ishikawa J et al. Acute peritonitis and salpingitis associated with streptococcal toxic shock syndrome caused by Lancefield group G alpha-haemolytic Streptococcus dysgalactiae subsp. equisimilis . J Med Microbiol 2006; 55:953–956 [CrossRef][PubMed]
    [Google Scholar]
  18. Zhao J, Hayashi T, Saarinen S, Papageorgiou AC, Kato H et al. Cloning, expression, and characterization of the superantigen streptococcal pyrogenic exotoxin G from Streptococcus dysgalactiae . Infect Immun 2007; 75:1721–1729 [CrossRef][PubMed]
    [Google Scholar]
  19. Shannon BA, McCormick JK, Schlievert PM. Toxins and superantigens of group A streptococci. Microbiol Spectr 2019; 7: [CrossRef][PubMed]
    [Google Scholar]
  20. Ahmad Y, Gertz RE, Li Z, Sakota V, Broyles LN et al. Genetic relationships deduced from emm and multilocus sequence typing of invasive Streptococcus dysgalactiae subsp. equisimilis and S. canis recovered from isolates collected in the United States. J Clin Microbiol 2009; 47:2046–2054 [CrossRef][PubMed]
    [Google Scholar]
  21. Genteluci GL, Silva LG, Souza MC, Glatthardt T, de Mattos MC et al. Assessment and characterization of biofilm formation among human isolates of Streptococcus dysgalactiae subsp. equisimilis . Int J Med Microbiol 2015; 305:937–947 [CrossRef][PubMed]
    [Google Scholar]
  22. Tibayrenc M, Ayala FJ. Reproductive clonality of pathogens: a perspective on pathogenic viruses, bacteria, fungi, and parasitic protozoa. Proc Natl Acad Sci U S A 2012; 109:E3305–E3313 [CrossRef][PubMed]
    [Google Scholar]
  23. Amaral MM, Coelho LR, Flores RP, Souza RR, Silva-Carvalho MC et al. The predominant variant of the Brazilian epidemic clonal complex of methicillin-resistant Staphylococcus aureus has an enhanced ability to produce biofilm and to adhere to and invade airway epithelial cells. J Infect Dis 2005; 192:801–810 [CrossRef][PubMed]
    [Google Scholar]
  24. Chien Y-W, Vidal JE, Grijalva CG, Bozio C, Edwards KM et al. Density interactions among Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus in the nasopharynx of young Peruvian children. Pediatr Infect Dis J 2013; 32:72–77 [CrossRef][PubMed]
    [Google Scholar]
  25. Alves-Barroco C, Roma-Rodrigues C, Raposo LR, Brás C, Diniz M et al. Streptococcus dysgalactiae subsp. dysgalactiae isolated from milk of the bovine udder as emerging pathogens: In vitro and in vivo infection of human cells and zebrafish as biological models. Microbiology Open 2019; 8:e00623 [CrossRef][PubMed]
    [Google Scholar]
  26. Rato MG, Nerlich A, Bergmann R, Bexiga R, Nunes SF et al. 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 2011; 49:2470–2479 [CrossRef][PubMed]
    [Google Scholar]
  27. Wood WB. The Nematode Caenorhabditis elegans New York: Cold Spring Harbor Laboratory Press; 1988 p 587
    [Google Scholar]
  28. Garsin DA, Sifri CD, Mylonakis E, Qin X, Singh KV et al. A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci U S A 2001; 98:10892–10897 [CrossRef][PubMed]
    [Google Scholar]
  29. Zhang Y, Lu H, Bargmann CI. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans . Nature 2005; 438:179–184 [CrossRef][PubMed]
    [Google Scholar]
  30. Silva-Filho RG. Propriedades de Streptococcus do grupo B crescido in vivo usando câmaras permeáveis intraperitoneais Universidade Federal do Rio de Janeiro; 1991
    [Google Scholar]
  31. Corrêa AB de A, Silva LG da, Pinto T de CA, Oliveira ICM de, Fernandes FG et al. The genetic diversity and phenotypic characterisation of Streptococcus agalactiae isolates from Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 2011; 106:1002–1006 [CrossRef][PubMed]
    [Google Scholar]
  32. de Melo MCN, Sá Figueiredo AM, Ferreira-Carvalho BT. Antimicrobial susceptibility patterns and genomic diversity in strains of Streptococcus pyogenes isolated in 1978-1997 in different Brazilian cities. J Med Microbiol 2003; 52:251–258 [CrossRef][PubMed]
    [Google Scholar]
  33. Maeda Y, Elborn JS, Parkins MD, Reihill J, Goldsmith CE et al. Population structure and characterization of viridans group streptococci (VGS) including Streptococcus pneumoniae isolated from adult patients with cystic fibrosis (CF). J Cyst Fibros 2011; 10:133–139 [CrossRef][PubMed]
    [Google Scholar]
  34. Sierra JM, Sánchez F, Castro P, Salvadó M, de la Red G et al. Group A streptococcal infections in injection drug users in Barcelona, Spain. Medicine 2006; 85:139–146 [CrossRef]
    [Google Scholar]
  35. Yin J, Yu S, Liu X, Li Y, Gao W et al. Molecular characterization of group G Streptococcus dysgalactiae subsp. equisimilis recovered from patients and healthy people in China. Diagn Microbiol Infect Dis 2012; 72:41–46 [CrossRef][PubMed]
    [Google Scholar]
  36. Pinho MD, Melo-Cristino J, Ramirez M. Clonal relationships between invasive and noninvasive Lancefield group C and G streptococci and emm-specific differences in invasiveness. J Clin Microbiol 2006; 44:841–846 [CrossRef][PubMed]
    [Google Scholar]
  37. Lu B, Fang Y, Huang L, Diao B, Du X et al. Molecular characterization and antibiotic resistance of clinical Streptococcus dysgalactiae subsp. equisimilis in Beijing, China. Infect Genet Evol 2016; 40:119–125 [CrossRef][PubMed]
    [Google Scholar]
  38. Oppegaard O, Mylvaganam H, Skrede S, Lindemann PC, Kittang BR. Emergence of a Streptococcus dysgalactiae subspecies equisimilis stG62647-lineage associated with severe clinical manifestations. Sci Rep 2017; 7:7589 [CrossRef][PubMed]
    [Google Scholar]
  39. Watanabe S, Kirikae T, Miyoshi-Akiyama T. Complete genome sequence of Streptococcus dysgalactiae subsp. equisimilis 167 carrying Lancefield group C antigen and comparative genomics of S. dysgalactiae subsp. equisimilis strains. Genome Biol Evol 2013; 5:1644–1651 [CrossRef][PubMed]
    [Google Scholar]
  40. Sánchez-Diener I, Zamorano L, López-Causapé C, Cabot G, Mulet X et al. Interplay among resistance profiles, high-risk clones, and virulence in the Caenorhabditis elegans Pseudomonas aeruginosa infection model. Antimicrob Agents Chemother 2017; 61:e01586–17 [CrossRef][PubMed]
    [Google Scholar]
  41. Day SR, Moore CM, Kundzins JR, Sifri CD. Community-associated and healthcare-associated methicillin-resistant Staphylococcus aureus virulence toward Caenorhabditis elegans compared. Virulence 2012; 3:576–582 [CrossRef][PubMed]
    [Google Scholar]
  42. Siemens N, Kittang BR, Chakrakodi B, Oppegaard O, Johansson L et al. Increased cytotoxicity and streptolysin O activity in group G streptococcal strains causing invasive tissue infections. Sci Rep 2015; 5:16945 [CrossRef][PubMed]
    [Google Scholar]
  43. Gleich-Theurer U, Aymanns S, Haas G, Mauerer S, Vogt J et al. Human serum induces streptococcal C5a peptidase expression. Infect Immun 2009; 77:3817–3825 [CrossRef][PubMed]
    [Google Scholar]
  44. Strus M, Heczko PB, Golińska E, Tomusiak A, Chmielarczyk A et al. The virulence factors of group A Streptococcus strains isolated from invasive and non-invasive infections in Polish and German centres, 2009-2011. Eur J Clin Microbiol Infect Dis 2017; 36:1643–1649 [CrossRef][PubMed]
    [Google Scholar]
  45. McMillan DJ, Bessen DE, Pinho M, Ford C, Hall GS et al. Population genetics of Streptococcus dysgalactiae subspecies equisimilis reveals widely dispersed clones and extensive recombination. PLoS One 2010; 5:e11741 [CrossRef][PubMed]
    [Google Scholar]
  46. Hashikawa S, Iinuma Y, Furushita M, Ohkura T, Nada T et al. Characterization of group C and G streptococcal strains that cause streptococcal toxic shock syndrome. J Clin Microbiol 2004; 42:186–192 [CrossRef][PubMed]
    [Google Scholar]
  47. Tseng S-P, Lin Y-Y, Tsai J-C, Hsueh P-R, Chen H-J et al. Distribution of emm types and genetic characterization of the mgc locus in group G Streptococcus dysgalactiae subsp. equisimilis from a hospital in Northern Taiwan. J Clin Microbiol 2010; 48:2975–2977 [CrossRef][PubMed]
    [Google Scholar]
  48. McDonald M, Towers RJ, Andrews RM, Carapetis JR, Currie BJ. Epidemiology of Streptococcus dysgalactiae subsp. equisimilis in tropical communities, Northern Australia. Emerg Infect Dis 2007; 13:1694–1700 [CrossRef][PubMed]
    [Google Scholar]
  49. Albertí S, García-Rey C, García-Laorden MI, Dal-Ré R, García-de-Lomas J et al. Survey of emm-like gene sequences from pharyngeal isolates of group C and group G streptococci collected in Spain. J Clin Microbiol 2005; 43:1433–1436 [CrossRef][PubMed]
    [Google Scholar]
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