• Authors: Dmitriev AV1,2, Kisely ov AM3, Kireeva AG1, Il’yasov Y.Y.1, Sergushichev AA4, Kazakov SV4, Kalinina OV3,5
  • Affiliations:
    1. Institute of Experimental Medicine
    2. St. Petersburg State Technological Institute (Technical University)
    3. Almazov North-West Federal Medical Research Centre
    4. ITMO University
    5. St. Petersburg Pasteur Institute
  • Issue: Vol 16, No 2 (2016)
  • Pages: 42-50
  • Section: Articles
  • URL:
  • DOI:
  • Cite item
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Streptococcus dysgalactiae subsp. equisimilis (SDSE) previously considered to be a commensal bacterium, is currently recognized as a causative agent of about 60% of infections caused by groups C and G streptococci. Goal of the present study was to search the novel genetic determinants in the genome of four SDSE strains using next generation sequencing and bioinformatic analysis. As result, genome sequences of four SDSE strains were determined, and numerous DNA fragments previously uncharacterized for SDSE were revealed. Most of the fragments were presented by migrating genetic elements such as bacteriophages, transposons, plasmids, integrative conjugative elements etc. For the first time the resistance genes to antibacterial drugs (tetS, tetT - resistance to tetracycline, and lsaE, lnuB - to lincosamides) were determined in the studied SDSE strains. Given that horizontal gene transfer, in particular, virulence genes associated with migrating genetic elements, is a driving force of streptococcal evolution, an emergence of novel virulent SDSE clones is expected.

A V Dmitriev

Institute of Experimental Medicine; St. Petersburg State Technological Institute (Technical University)

St. Petersburg, Russia

A M Kisely ov

Almazov North-West Federal Medical Research Centre

St. Petersburg, Russia

A G Kireeva

Institute of Experimental Medicine

St. Petersburg, Russia

Yu Yu Il’yasov

Institute of Experimental Medicine

St. Petersburg, Russia

A A Sergushichev

ITMO University

St. Petersburg, Russia

S V Kazakov

ITMO University

St. Petersburg, Russia

O V Kalinina

Almazov North-West Federal Medical Research Centre; St. Petersburg Pasteur Institute

St. Petersburg, Russia

  1. Vandamme P., Pot B., Falsen E., Kersters K., Devriese L. A. Taxonomic study of Lancefield streptococcal groups C, G, and L (Streptococcus dysgalactiae) and Proposal of S. dysgalactiae subsp. equisimilis subsp. nov. // Int. J. Syst. Bacteriol.- 1996.- Vol. 46.- P. 774-781.
  2. Takahashi T., Sunaoshi K., Sunakawa K., Fujishima S., Watanabe H., Ubukata K. Invasive streptococcal disease Working Group. Clinical aspects of invasive infections with Streptococcus dysgalactiae ssp. equisimilis in Japan: differences with respect to Streptococcus pyogenes and Streptococcus agalactiae infections // Clin. Microbiol. Infect.- 2010.- Vol. 16, № 8.- P. 1097-1103.
  3. Brandt C. M., Spellerberg B. Human infections due to Streptococcus dysgalactiae subspecies equisimilis // Clin. Infect. Dis.- 2009.- Vol. 49, № 5.- P. 766-772.
  4. Suzuki H., Lefebure T., Hubisz M. J., Bitar P. P., Lang P., Siepel A., Stanhope M. J. Comparative genomic analysis of the Streptococcus dysgalactiae species group: gene content, molecular adaptation, and promoter evolution // Genome Biol. Evol.- 2011.- Vol. 3.- P. 168-185.
  5. Hashikawa S., Iinuma Y., Furushita M., Ohkura T., Nada T., Torii K., Hasegawa T., Ohta M. Characterization of group C and G streptococcal strains that cause streptococcal toxic shock syndrome // J. Clin. Microbiol.- 2004.- Vol. 42, № 1.- P. 186-192.
  6. Wajima T., Morozumi M., Hanada S., Sunaoshi K., Chiba N., Iwata S., Ubukata K. Molecular characterization of invasive Streptococcus dysgalactiae subsp. equisimilis, Japan // Emerg. Infect. Dis.- 2016.- Vol. 22, № 2 - P. 247-254.
  7. Okumura K., Shimomura Y., Murayama S. Y., Yagi J., Ubukata K., Kirikae T., Miyoshi-Akiyama T. Evolutionary paths of streptococcal and staphylococcal superantigens // BMC Genomics.- 2012.- doi: 10.1186/1471-2164-13-404.
  8. 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.- Vol. 5, № 9.- P. 1644-1651.
  9. Shimomura Y., Okumura K., Murayama S.Y., Yagi J., Ubukata K., Kirikae T., Miyoshi-Akiyama T. Complete genome sequencing and analysis of a Lancefield group G Streptococcus dysgalactiae subsp. equisimilis strain causing streptococcal toxic shock syndrome (STSS) // BMC Genomics.- 2011.- doi: 10.1186/1471-2164-12-17.
  10. Bessen D. E., McShan W. M., Nguyen S. V., Shetty A., Agrawal S., Tettelin H. Molecular epidemiology and genomics of group A Streptococcus // Infection, Genetics and Evolution.- 2015.- Vol. 33.- P. 393-418.
  11. McNeilly C. L., McMillan D. J. Horizontal gene transfer and recombination in Streptococcus dysgalactiae subsp equisimilis // Front. Microbiology.- 2014.- Vol. 5.- Р. 676.- doi: 10.3389.
  12. Носик А. Г., Ильясов Ю. Ю., Линь Ф. К., Дмитриев А. В. Молекулярно-эпидемиологическая характеристика стрептококков, выделенных у детей младшего школьного возраста во Вьетнаме // Журн. инфектологии.- 2015.- Т. 7, № 3.- С. 112-118.
  13. Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., Lesin V. M., Nikolenko S. I., Pham S., Prjibelski A. D., Pyshkin A. V., Sirotkin A. V., Vyahhi N., Tesler G., Alekseyev M. A., Pevzner P. A. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing // J. Comput. Biol.- 2012.- Vol. 19, № 5.- P. 455-477.
  14. Montilla A., Zavala A., Caceres R., Cittadini R., Vay C., Gutkind G., Famiglietti A., Bonofiglio L., Mollerach M. Genetic Environment of the lnu(B) gene in a Streptococcus agalactiae clinical isolate // Antimicrob. Agents Chemother.- 2014.- Vol. 58, № 9.- P. 5636-5637.
  15. Brenciani A., Bacciaglia A., Vignaroli C., Pugnaloni A., Varaldo P. E., Giovanetti E. Phim46.1, the main Streptococcus pyogenes element carrying mef(A) and tet(O) genes // Antimicrob. Agents Chemother.- 2010.- Vol. 54, № 1.- P. 221-229.
  16. Tang F., Bossers A., Harders F., Lu C., Smith H. Comparative genomic analysis of twelve Streptococcus suis (pro)phages // Genomics.- 2013.- Vol. 101, № 6.- P. 336-344.
  17. Port G. C., Paluscio E., Caparon M. G. Complete genome sequences of emm6 Streptococcus pyogenes JRS4 and parental strain D471 // Genome Announc.- 2015.- Vol. 3, № 4.- Р. 00725-15.
  18. Da Cunha V., Davies M. R., Douarre P. E., Rosinski-Chupin I., Margarit I., Spinali S., Perkins T., Lechat P., Dmytruk N., Sauvage E., Ma L., Romi B., Tichit M., Lopez-Sanchez M. J., Descorps-Declere S., Souche E., Buchrieser C., Trieu-Cuot P., Moszer I., Clermont D., Maione D., Bouchier C., McMillan D. J., Parkhill J., Telford J. L., Dougan G., Walker M. J., Holden M. T. G., Poyart C., Glaser P., Melin P., Decheva A., Petrunov B., Kriz P., Berner R., Buchele A., Hufnagel M., Kunze M., Creti R., Baldassari L., Orefici G., Berardi A., Granger J. R., Fraile M. D., Afshar B., Efstratiou A. Streptococcus agalactiae clones infecting humans were selected and fixed through the extensive use of tetracycline // Nat. Commun.- 2014.- Vol. 5 - P. 4544.
  19. Solheim M., Aakra A., Snipen L. G., Brede D. A., Nes I. F. Comparative genomics of Enterococcus faecalis from healthy Norwegian infants // BMC Genomics.- 2009.- doi: 10.1186/1471-2164-10-194.
  20. Wang R., Li L., Luo F., Liang W., Gan X., Chen M. Genome sequence of Streptococcus agalactiae strain H002, serotype III, isolated in China from a pregnant woman // Genome Announc.- 2015.- Vol. 3, № 5.- Р. 01109-01115.
  21. de Andrade Barboza S., Meygret A., Vincent P., Moullec S., Soriano N., Lagente V., Minet J., Kayal S., Faili A. Complete genome sequence of noninvasive Streptococcus pyogenes M/emm28 strain STAB10015, isolated from a child with perianal dermatitis in French Brittany // Genome Announc.- 2015.- Vol. 3, № 4.- Р. 00806-00815.
  22. Athey T. B., Auger J. P., Teatero S., Dumesnil A., Takamatsu D., Wasserscheid J., Dewar K., Gottschalk M., Fittipaldi N. Complex population structure and virulence differences among serotype 2 Streptococcus suis strains belonging to Sequence Type 28 // PLoS ONE.- 2015.- Vol. 10, №9.- Р. 0137760.
  23. Tettelin H., Masignani V., Cieslewicz M. J. Eisen J. A., Peterson S., Wessels M. R., Paulsen I. T., Nelson K. E., Margarit I., Read T. D., Madoff L. C., Wolf A. M., Beanan M. J., Brinkac L. M., Daugherty S. C., DeBoy R. T., Durkin A. S., Kolonay J. F., Madupu R., Lewis M. R., Radune D., Fedorova N. B., Scanlan D., Khouri H., Mulligan S., Carty H. A., Cline R. T., Van Aken S. E., Gill J., Scarselli M., Mora M., Iacobini E. T., Brettoni C., Galli G., Mariani M., Vegni F., Maione D., Rinaudo D., Rappuoli R., Telford J. L., Kasper D. L., Grandi G., Fraser C. M. Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae // Proc. Natl. Acad. Sci. U.S.A.- 2002.- Vol. 99, № 19.- P. 12391-12396.
  24. Tettelin H., Masignani V., Cieslewicz M. J., Donati C., Medini D., Ward N. L., Angiuoli S. V., Crabtree J., Jones A. L., Durkin A. S., DeBoy R. T., Davidsen T. M., Mora M., Scarselli M., Ros I. M. Y., Peterson J. D., Hauser C. R., Sundaram J. P., Nelson W. C., Madupu R., Brinkac L. M., Dodson R. J., Rosovitz M. J., Sullivan S. A., Daugherty S. C., Haft D. H., Selengut J., Gwinn M. L., Zhou L. W., Zafar N., Khouri H., Radune D., Dimitrov G., Watkins K., O’Connor K. J. B., Smith S., Utterback T. R., White O., Rubens C.E., Grandi G., Madoff L. C., Kasper D. L., Telford J. L., Wessels M. R., Rappuoli R., Fraser C. M. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial ‘pan-genome’ // Proc. Natl. Acad. Sci. U.S.A.- 2005.- Vol. 102, № 39.- P. 13950-13955.
  25. Lin I. H., Liu T. T., Teng Y.T., Wu H. L., Liu Y. M., Wu K. M., Chang C. H., Hsu M. T. Sequencing and comparative genome analysis of two pathogenic Streptococcus gallolyticus subspecies: genome plasticity, adaptation and virulence // PLoS ONE.- 2011.- Vol. 6, № 5.- Р. 20519.
  26. Beres S. B., Richter E. W., Nagiec M. J., Sumby P., Porcella S. F., Deleo F. R., Musser J. M. Molecular genetic anatomy of inter- and intraserotype variation in the human bacterial pathogen group A Streptococcus // Proc. Natl. Acad. Sci. U.S.A.- 2006.- Vol. 103, № 18 - P. 7059-7064.
  27. Holden M. T., Heather Z., Paillot R., Steward K. F., Webb K., Ainslie F., Jourdan T., Bason N. C., Holroyd N. E., Mungall K., Quail M. A., Sanders M., Simmonds M., Willey D., Brooks K., Aanensen D. M., Spratt B. G., Jolley K. A., Maiden M. C. J., Kehoe M., Chanter N., Bentley S. D., Robinson C., Maskell D. J., Parkhill J., Waller A. S. Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens // PLoS. Pathog.- 2009.- Vol. 5, № 3.- Р. 1000346.
  28. Brenciani A., Tiberi E., Bacciaglia A., Petrelli D., Varaldo P. E., Giovanetti E. Two distinct genetic elements are responsible for erm(TR)-medi- ated erythromycin resistance in tetracycline-susceptible and tetracycline-resistant strains of Streptococcus pyogenes / / Antimicrob. Agents Chemother.- 2011.- Vol. 55, № 5.- P. 2106-2112.
  29. Zubair S., de Villiers E. P., Younan M., Andersson G., Tettelin H., Riley D. R., Jores J., Bongcam-Rudloff E., Bishop R. P. Genome sequences of two pathogenic Streptococcus agalactiae isolates from the one-humped camel Camelus dromedaries // Genome Announc.- 2013.- Vol. 1, № 4.- Р. 00515-00513.
  30. Clermont D., Chesneau O., De Cespedes G., Horaud T. New tetracycline resistance determinants coding for ribosomal protection in streptococci and nucleotide sequence of tet(T) isolated from Streptococcus pyogenes A498 // Antimicrob. Agents Chemother.- 1997.- Vol. 41, № 1.- P. 112-116.
  31. Nakagawa I., Kurokawa K., Yamashita A., Nakata M., Tomiyasu Y., Okahashi N., Kawabata S., Yamazaki K., Shiba T., Yasunaga T., Hayashi H., Hattori M., Hamada S. Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolution // Genome Res.- 2003.- Vol. 13, № 6A.- P. 1042-1055.
  32. Davies M. R., McMillan D. J., Van Domselaar G. H., Jones M. K., Sriprakash K. S. Phage 3396 from a Streptococcus dysgalactiae subsp. equisimilis pathovar may have its origins in Streptococcus pyogenes // J. Bacteriol.- 2007.- Vol. 189, № 7.- P. 2646-2652.
  33. Benson M. A., Ohneck E. A., Ryan C., Alonzo F., Smith H., Narechania A., Kolokotronis S. O., Satola S. W., Uhlemann A. C., Sebra R., Deikus G., Shopsin B., Planet P. J., Torres V. J. Evolution of hypervirulence by a MRSA clone through acquisition of a transposable element // Mol. Microbiol.- 2014.- Vol. 93, № 4.- P. 664-681.


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