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Population structure and virulence gene profiles of Streptococcus agalactiae collected from different hosts worldwide

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Abstract

Streptococcus agalactiae is a leading cause of morbidity and mortality among neonates and causes severe infections in pregnant women and nonpregnant predisposed adults, in addition to various animal species worldwide. Still, information on the population structure of S. agalactiae and the geographical distribution of different clones is limited. Further data are urgently needed to identify particularly successful clones and obtain insights into possible routes of transmission within one host species and across species borders. We aimed to determine the population structure and virulence gene profiles of S. agalactiae strains from a diverse set of sources and geographical origins. To this end, 373 S. agalactiae isolates obtained from humans and animals from five different continents were typed by DNA microarray profiling. A total of 242 different S. agalactiae strains were identified and further analyzed. Particularly successful clonal lineages, hybridization patterns, and strains were identified that were spread across different continents and/or were present in more than one host species. In particular, several strains were detected in both humans and cattle, and several canine strains were also detected in samples from human, bovine, and porcine hosts. The findings of our study suggest that although S. agalactiae is well adapted to various hosts including humans, cattle, dogs, rodents, and fish, interspecies transmission is possible and occurs between humans and cows, dogs, and rabbits. The virulence and resistance gene profiles presented enable new insights into interspecies transmission and make a crucial contribution to the identification of suitable targets for therapeutic agents and vaccines.

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References

  1. Krohn MA, Hillier SL, Baker CJ (1999) Maternal peripartum complications associated with vaginal group B Streptococci colonization. J Infect Dis 179:1410–1415

    Article  CAS  PubMed  Google Scholar 

  2. Farley M, Harvey C, Stull T et al (1993) A population-based assessment of invasive disease due to group B Streptococcus in nonpregnant adults. N Engl J Med 328:1807–1811

    Article  CAS  PubMed  Google Scholar 

  3. Jackson LA, Hilsdon R, Farley MM et al (1995) Risk factors for group B streptococcal disease in adults. Ann Intern Med 123:415–420

    Article  CAS  PubMed  Google Scholar 

  4. Van der Mee-Marquet N, Domelier A-S, Salloum M et al (2009) Molecular characterization of temporally and geographically matched Streptococcus agalactiae strains. Foodborne Pathog Dis 6:1177–1183

    Article  PubMed  Google Scholar 

  5. Foxman B, Gillespie BW, Manning SD, Marrs CF (2007) Risk factors for group B streptococcal colonization: potential for different transmission systems by capsular type. Ann Epidemiol 17:854–862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hetzel U, König A, Yildirim AÖ, Lämmler C, Kipar A (2003) Septicaemia in emerald monitors (Varanus prasinus Schlegel 1839) caused by Streptococcus agalactiae acquired from mice. Vet Microbiol 95:283–293

    Article  CAS  PubMed  Google Scholar 

  7. Duremdez R, Al-Marzouk A, Qasem JA, Al-Harbi A, Gharabally H (2004) Isolation of Streptococcus agalactiae from cultured silver pomfret, Pampus argenteus (Euphrasen), in Kuwait. J Fish Dis 27:307–310

    Article  CAS  PubMed  Google Scholar 

  8. Barkema HW, Green MJ, Bradley AJ, Zadoks RN (2009) Invited review: the role of contagious disease in udder health. J Dairy Sci 92:4717–4729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Keefe G (2012) Update on control of Staphylococcus aureus and Streptococcus agalactiae for management of mastitis. Vet Clin North Am Food Anim Pract 28:203–216

    Article  PubMed  Google Scholar 

  10. Le Doare K, Heath PT (2013) An overview of global GBS epidemiology. Vaccine 31:D7–12

    Article  PubMed  Google Scholar 

  11. Johri AK, Paoletti LC, Glaser P, Dua M, Sharma PK, Grandi G et al (2006) Group B Streptococcus: global incidence and vaccine development. Nat Rev Microbiol 4:932–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Nuccitelli A, Rinaudo CD, Maione D (2015) Group B Streptococcus vaccine: state of the art. Ther Adv Vaccines 3:76–90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Nitschke H, Slickers P, Müller E, Ehricht R, Monecke S (2014) DNA microarray-based typing of Streptococcus agalactiae. J Clin Microbiol 52:3933–3943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Yao K, Poulsen K, Maione D et al (2013) Capsular gene typing of Streptococcus agalactiae compared to serotyping by latex agglutination. J Clin Microbiol 51:503–507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Yildirim AÖ, Lämmler C, Weiß R (2002) Identification and characterization of Streptococcus agalactiae isolated from horses. Vet Microbiol 85:31–35

    Article  CAS  PubMed  Google Scholar 

  16. Skov Sørensen UB, Poulsen K, Ghezzo C, Margarit I, Kilian M (2010) Emergence and global dissemination of host-specific Streptococcus agalactiae clones. MBio 1:1–9

    Article  Google Scholar 

  17. Delannoy CM, Crumlish M, Fontaine MC et al (2013) Human Streptococcus agalactiae strains in aquatic mammals and fish. BMC Microbiol 13:41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ip M, Cheuk ESC, Tsui MHY, Kong F, Leung TN, Gilbert GL (2006) Identification of a Streptococcus agalactiae serotype III subtype 4 clone in association with adult invasive disease in Hong Kong. J Clin Microbiol 44:4252–4254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Belard S, Toepfner N, Capan-Melser M et al (2015) Streptococcus agalactiae serotype distribution and antimicrobial susceptibility in pregnant women in Gabon, Central Africa. Sci Rep 5:17281

    Article  PubMed  PubMed Central  Google Scholar 

  20. Manning SD, Springman AC, Million AD et al. (2010) Association of group B Streptococcus colonization and bovine exposure: a prospective cross-sectional cohort study. PLoS One 5(1):e8795

    Article  PubMed  PubMed Central  Google Scholar 

  21. Ashrafian H, Griselli M, Rubens MB, Mullen MJ, Sethia B (2007) Pulmonary homograft endocarditis 19 years after a Ross procedure. Thorac Cardiovasc Surg 55:55–56

    Article  CAS  PubMed  Google Scholar 

  22. Bishop EJ, Shilton C, Benedict S et al (2007) Necrotizing fasciitis in captive juvenile Crocodylus porosus caused by Streptococcus agalactiae: an outbreak and review of the animal and human literature. Epidemiol Infect 135:1248–1255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Dogan B, Schukken YH, Santisteban C, Boor J, Boor KJ (2005) Distribution of serotypes and antimicrobial resistance genes among Streptococcus agalactiae isolates from bovine and human hosts. Society 43:5899–5906

    CAS  Google Scholar 

  24. Oliveira ICM, De Mattos MC, Pinto TA, Benchetrit LC (2006) Genetic relatedness between group B Streptococci originating from bovine mastitis and a human group B Streptococcus type V cluster displaying an identical pulsed-field gel electrophoresis pattern. Clin Microbiol Infect 12:887–893

    Article  CAS  PubMed  Google Scholar 

  25. Lee S, Roh KH, Kim CK et al (2008) A case of necrotizing fasciitis due to Streptococcus agalactiae, Arcanobacterium haemolyticum, and Finegoldia magna in a dog-bitten patient with diabetes. Korean J Lab Med 28:191–195

    Article  CAS  PubMed  Google Scholar 

  26. Chen M, Wang R, Luo FG et al (2015) Streptococcus agalactiae isolates of serotypes Ia, III and V from human and cow are able to infect tilapia. Vet Microbiol 180:129–135

    Article  PubMed  Google Scholar 

  27. Evans JJ, Klesius PH, Pasnik DJ, Bohnsack JF (2009) Human Streptococcus agalactiae isolate in nile tilapia (Oreochromis niloticus). Emerg Infect Dis 15:774–776

    Article  PubMed  PubMed Central  Google Scholar 

  28. Pereira UP, Mian GF, Oliveira ICM, Benchetrit LC, Costa GM, Figueiredo HCP (2010) Genotyping of Streptococcus agalactiae strains isolated from fish, human and cattle and their virulence potential in Nile tilapia. Vet Microbiol 140:186–192

    Article  CAS  PubMed  Google Scholar 

  29. Coombs GW, Monecke S, Ehricht R et al (2010) Differentiation of clonal complex 59 community-associated methicillin-resistant Staphylococcus aureus in Western Australia. Antimicrob Agents Chemother 54:1914–1921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  CAS  PubMed  Google Scholar 

  31. Wattinger L, Stephan R, Layer F, Johler S (2012) Comparison of Staphylococcus aureus isolates associated with food intoxication with isolates from human nasal carriers and human infections. Eur J Clin Microbiol Infect Dis 31:455–464

    Article  CAS  PubMed  Google Scholar 

  32. Kalimuddin S, Chen SL, Lim CTK et al. (2017) 2015 epidemic of severe Streptococcus agalactiae sequence type 283 infections in Singapore associated with the consumption of raw freshwater fish: a detailed analysis of clinical, epidemiological, and bacterial sequencing data. Clin Infect Dis 64(2):S145–S152

  33. Lindahl G, Stålhammar-Carlemalm M, Areschoug T (2005) Surface proteins of Streptococcus agalactiae and related proteins in other bacterial pathogens. Clin Microbiol Rev 18:102–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Bolukaoto JY, Monyama CM, Chukwu MO et al (2015) Antibiotic resistance of Streptococcus agalactiae isolated from pregnant women in Garankuwa. South Africa BMC Res Notes 8:364

    Article  PubMed  Google Scholar 

  35. Creti R, Imperi M, Berardi A et al (2017) Neonatal group B Streptococcus infections. Pediatr Infect Dis J 36:256–262

    Article  PubMed  Google Scholar 

  36. Rojo-Bezares B, Azcona-Gutiérrez JM, Martin C, Jareño MS, Torres C, Sáenz Y (2016) Streptococcus agalactiae from pregnant women: antibiotic and heavy-metal resistance mechanisms and molecular typing. Epidemiol Infect 144:3205–3214

    Article  CAS  PubMed  Google Scholar 

  37. Areschoug T, Linse S, Stålhammar-Carlemalm M, Hedén LO, Lindahl G (2002) A proline-rich region with a highly periodic sequence in streptococcal beta protein adopts the polyproline II structure and is exposed on the bacterial surface. J Bacteriol 184:6376–6383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Nagano N, Nagano Y, Taguchi F (2002) High expression of a C protein beta antigen gene among invasive strains from certain clonally related groups of type Ia and Ib group B Streptococci. Infect Immun 70:4643–4649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kong F, Gidding HF, Berner R, Gilbert GL (2006) Streptococcus agalactiae Cβ protein gene (bac) sequence types, based on the repeated region of the cell-wall-spanning domain: relationship to virulence and a proposed standardized nomenclature. J Med Microbiol 55:829–837

    Article  CAS  PubMed  Google Scholar 

  40. Maeland JA, Afset JE, Lyng RV, Radtke A (2015) Survey of immunological features of the alpha-like proteins of Streptococcus agalactiae. Clin Vaccine Immunol 22:153–159

    Article  PubMed  PubMed Central  Google Scholar 

  41. Springman A, Lacher DW, Waymire EA et al (2014) Pilus distribution among lineages of group b Streptococcus: an evolutionary and clinical perspective. BMC Microbiol 14:159

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the Institute of Medical Microbiology, University of Zurich, for providing strains.

Funding

All materials used for this study were funded by the Institute for Food Safety, University of Zurich. No third-party funding or external grants were involved.

Author information

Authors and Affiliations

  1. Institute for Food Safety and Hygiene, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 272, 8057, Zurich, Switzerland

    Marina Morach, Roger Stephan & Sophia Johler

  2. Institute of Veterinary Bacteriology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland

    Sarah Schmitt

  3. Institute of Hygiene and Infectious Diseases in Animals, Justus-Liebig University, Giessen, Germany

    Christa Ewers

  4. Hessian State Laboratory, Department of Veterinary Medicine, Giessen, Germany

    Michael Zschöck

  5. Department of Health Management, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PE, Canada

    Julian Reyes-Velez

  6. Tropical Medicine Institute of Colombia, Tropical Medicine Research Group, Antonio Roldan Betancur—CES University, Medellin, Colombia

    Julian Reyes-Velez

  7. IDEXX Diavet Laboratories, Bäch, Switzerland

    Urs Gilli

  8. Department of Microbiology, University of Valle, Cali, Colombia

    María del Pilar Crespo-Ortiz

  9. Department of Biomedical Sciences, Santiago de Cali University, Cali, Colombia

    María del Pilar Crespo-Ortiz

  10. Institute of Aquaculture, University of Stirling, Stirling, UK

    Margaret Crumlish

  11. Aga Khan University Hospital, Nairobi, Kenya

    Revathi Gunturu

  12. Swiss Tropical and Public Health Institute, Basel, Switzerland

    Claudia A. Daubenberger

  13. University of Basel, Basel, Switzerland

    Claudia A. Daubenberger

  14. Department of Microbiology, Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, Hong Kong, China

    Margaret Ip

  15. labor-zentral.ch, Geuensee, Switzerland

    Walter Regli

Authors
  1. Marina Morach
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  2. Roger Stephan
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  3. Sarah Schmitt
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  4. Christa Ewers
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  6. Julian Reyes-Velez
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  7. Urs Gilli
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  8. María del Pilar Crespo-Ortiz
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  9. Margaret Crumlish
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  10. Revathi Gunturu
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  11. Claudia A. Daubenberger
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  12. Margaret Ip
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  13. Walter Regli
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  14. Sophia Johler
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Corresponding author

Correspondence to Sophia Johler.

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Conflicts of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

Ethical approval

This study was carried out in accordance with ethical clearance and informed consent regulations of the locally cognizant ethics commission. All isolates were part of existing strain collections with anonymized sample information. No animal or human hosts were subjected to sampling for the purpose of the present study.

Informed consent

Formal consent was not required for this retrospective study.

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Morach, M., Stephan, R., Schmitt, S. et al. Population structure and virulence gene profiles of Streptococcus agalactiae collected from different hosts worldwide. Eur J Clin Microbiol Infect Dis 37, 527–536 (2018). https://doi.org/10.1007/s10096-017-3146-x

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  • DOI: https://doi.org/10.1007/s10096-017-3146-x

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