Genome diversity and evolutionary characteristics of clinical isolates of Bordetella pertussis circulating in Iran
-
Samaneh Saedi
,
Azadeh Safarchi
,
Mojtaba Noofeli
,
Keyvan Tadayon
,
Alfred Chin Yen Tay
,
Binit Lamichhane
,
Hamzeh Rahimi
,
Fereshteh Shahcheraghi
Abstract
Background and Objectives: The re-emergence of pertussis still is being reported all over the world. Pathogen adaptation and antigenic divergence of circulating isolates from vaccine strains are the main reasons of infection resurgence. Waning immunity is also an important factor contributing to resurgence of pertussis.
Materials and Methods: The genetic diversity and evolutionary characteristics of circulating Iranian isolates of Bordetella pertussis during February 2015 to October 2018 was investigated by pulsed-field gel electrophoresis (PFGE) and subsequently ptxA, ptxP and fim3 alleles were characterized. The next generation genome sequencing was then used to compare the genomics of ptxP1 and ptxP3 of selected isolates from PFGE dendrogram.
Results: PFGE differentiated 62 clinical isolates and vaccine and reference strains into 19 PFGE profiles, indicating the higher level of heterogeneity in the population during 2015-2018. The predominant B. pertussis genotype harbored pertussis toxin promoter allele, ptxP3 and the expansion of ptxA1 isolates, were also observed in our population.
Conclusion: No changes in allelic profile of predominant clone in recent years was observed but antigenic divergence between recently circulating isolates and the vaccine strain has been progressed and significantly was higher than previous studies. The comparative genomic analysis of the ptxP3 and ptxP1 isolates indicate that changes in ptxP3 genome structure including 32 unique SNPs and three unique indels may have contributed to the expansion of the ptxP3 clone. We compared ptxP3 and ptxP1 isolates in pathogenicity-associated genes and found five of them were specific for the ptxP3 isolates. The polymorphisms in pathogenicity-associated genes suggest structural adaptations for these virulence factors.
1. Clark TA. Changing pertussis epidemiology: everything old is new again. J Infect Dis 2014;209:978-981.
2. Advani A, Hallander HO, Dalby T, Krogfelt KA, Guiso N, Njamkepo E, et al. Pulsed-field gel electrophoresis analysis of Bordetella pertussis isolates circulating in Europe from 1998 to 2009. J Clin Microbiol 2013;51:422-428.
3. Winter K, Glaser C, Watt J, Harriman K, Centers for Disease Control and Prevention (CDC). Pertussis epidemic California, 2014. MMWR Morb Mortal Wkly Rep 2014;63:1129-1132.
4. Safarchi A, Octavia S, Wu SZ, Kaur S, Sintchenko V, Gilbert GL, et al. Genomic dissection of Australian Bordetella pertussis isolates from the 2008-2012 epidemic. J Infect 2016;72:468-477.
5. Sealey KL, Harris SR, Fry NK, Hurst LD, Gorringe AR, Parkhill J, et al. Genomic analysis of isolates from the United Kingdom 2012 pertussis outbreak reveals that vaccine antigen genes are unusually fast evolving. J Infect Dis 2015;212:294-301.
6. Cherry JD. Epidemic pertussis in 2012—the resurgence of a vaccine-preventable disease. N Engl J Med 2012;367:785-787.
7. Bart MJ, Harris SR, Advani A, Arakawa Y, Bottero D, Bouchez V, et al. Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. mBio 2014;5(2):e01074.
8. Bahmanjeh A, Noofeli M, Khaki P, Hassanzadeh SM. Genetic analysis of clinical and vaccine strains of Bordetella pertussis by pulsed-field gel electrophoresis (PFGE), multi locus sequence typing (MLST) and serotyping. Comp Immunol Microbiol Infect Dis 2019;64:168-175.
9. Dias W, van der Ark AA, Sakauchi MA, Kubrusly FS, Prestes AFR, Borges MM, et al. An improved whole cell pertussis vaccine with reduced content of endotoxin. Hum Vaccin Immunother 2013;9:339-348.
10. Moradi-Lakeh M, Esteghamati A. National immunization program in Iran: whys and why nots.Hum Vaccin Immunother 2013;9:112-114.
11. World Health Organization. WHO vaccine-preventable diseases: monitoring system 2013 global summary. 2013. Immunization schedule for. 2013;6.
12. Mooi FR. Bordetella pertussis and vaccination: the persistence of a genetically monomorphic pathogen. Infect Genet Evol 2010;10:36-49.
13. De Moissac Y, Ronald SL, Peppler MS. Use of pulsed-field gel electrophoresis for epidemiological study of Bordetella pertussis in a whooping cough outbreak. J Clin Microbiol 1994;32:398-402.
14. Bowden KE, Williams MM, Cassiday PK, Milton A, Pawloski L, Harrison M, et al. Molecular epidemiology of pertussis epidemic—Washington State, 2012. J Clin Microbiol 2014;52:3549-3557.
15. Weigand MR, Peng Y, Loparev V, Batra D, Bowden KE, Burroughs M, et al. The history of Bordetella pertussis genome evolution includes structural rearrangement. J Bacteriol 2017;199(8): e00806-00816.
16. Bart MJ, van Gent M, van der Heide HG, Boekhorst J, Hermans P, Parkhill J, et al. Comparative genomics of prevaccination and modern Bordetella pertussis strains. BMC Genomics 2010;11:627.
17. Belcher T, Preston A. Bordetella pertussis evolution in the (functional) genomics era. Pathog Dis 2015;73:ftv064.
18. Reischl U, Lehn N, Sanden GN, Loeffelholz MJ. Real-time PCR assay targeting IS481 of Bordetella pertussis and molecular basis for detecting Bordetella holmesii. J Clin Microbiol 2001;39:1963-1966.
19. Nikbin VS, Ahmadi NJ, Hosseinpour M, Lotfi MN, Shooraj F, Sadeghpour F, et al. Virulence factors variation among Bordetella pertussis isolates in Iran. Int J Mol Cell Med 2015;4:138-142.
20. Bottero D, Gaillard ME, Fingermann M, Weltman G, Fernández J, Sisti F, et al. Pulsed-field gel electrophoresis, pertactin, pertussis toxin S1 subunit polymorphisms, and surfaceome analysis of vaccine and clinical Bordetella pertussis strains. Clin Vaccine Immunol 2007;14:1490-1498.
21. Mooi FR, van Loo IH, Van Gent M, He Q, Bart MJ, Heuvelman KJ, et al. Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg Infect Dis 2009;15:1206-1213.
22. Haghighi F, Shahcheraghi F, Abbasi E, Eshraghi SS, Zeraati H, Mousavi SAJ, et al. Genetic profile variation in vaccine strains and clinical isolates of Bordetella pertussis recovered from Iranian patients. Avicenna J Med Biotechnol 2014;6:178-184.
23. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011;28:2731-2739.
24. Heravi FS, Nikbin VS, Lotfi MN, Badiri P, Ahmadi NJ, Zahraei SM, et al. Strain variation and antigenic divergence among Bordetella pertussis circulating strains isolated from patients in Iran. Eur J Clin Microbiol Infect Dis 2018;37:1893-1900.
25. Octavia S, Lan R. Frequent recombination and low level of clonality within Salmonella enterica subspecies I. Microbiology 2006;152:1099-1108.
26. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010;5(6):e11147.
27. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012;19:455-477.
28. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009;25:1754-1760.
29. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009;25:2078-2079.
30. Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, Harris DE, et al. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 2003;35:32-40.
31. Advani A, Donnelly D, Hallander H. Reference system for characterization of Bordetella pertussis pulsed-field gel electrophoresis profiles. J Clin Microbiol 2004;42:2890-2897.
32. Hallander H, Advani A, Riffelmann M, Von König CH, Caro V, Guiso N, et al. Bordetella pertussis strains circulating in Europe in 1999 to 2004 as determined by pulsed-field gel electrophoresis. J Clin Microbiol 2007;45:3257-3562.
33. Barkoff A-M, Mertsola J, Pierard D, Dalby T, Hoegh SV, Guillot S, et al. Surveillance of circulating Bordetella pertussis strains in Europe during 1998-2015. J Clin Microbiol 2018 Apr 25;56(5): e01998-02017.
34. Van Gent M, Heuvelman C, Van der Heide H, Hallander H, Advani A, Guiso N, et al. Analysis of Bordetella pertussis clinical isolates circulating in European countries during the period 1998–2012. Eur J Clin Microbiol Infect Dis 2015;34:821-830.
35. Shuel M, Jamieson FB, Tang P, Brown S, Farrell D, Martin I, et al. Genetic analysis of Bordetella pertussis in Ontario, Canada reveals one predominant clone. Int J Infect Dis 2013;17(6):e413-417.
36. Octavia S, Sintchenko V, Gilbert GL, Lawrence A, Keil AD, Hogg G, et al. Newly emerging clones of Bordetella pertussis carrying prn2 and ptxP3 alleles implicated in Australian pertussis epidemic in 2008–2010. J Infect Dis 2012;205:1220-1224.
37. Mosiej E, Augustynowicz E, Zawadka M, Dąbrowski W, Lutyńska A. Strain variation among Bordetella pertussis isolates circulating in Poland, after 50 years of whole-cell pertussis vaccine use. J Clin Microbiol 2011;49:1452-1457.
38. Polak M, Zasada AA, Mosiej E, Krysztopa-Grzybowska K, Witkowski L, Rzeczkowska M, et al. Pertactin-deficient Bordetella pertussis isolates in Poland—a country with whole-cell pertussis primary vaccination. Microbes Infect 2019;21:170-175.
39. de Gouw D, Hermans PW, Bootsma HJ, Zomer A, Heuvelman K, Diavatopoulos DA, et al. Differentially expressed genes in Bordetella pertussis strains belonging to a lineage which recently spread globally. PLoS One 2014;9(1):e84523.
40. King AJ, van der Lee S, Mohangoo A, van Gent M, van der Ark A, van de Waterbeemd B. Genome-wide gene expression analysis of Bordetella pertussis isolates associated with a resurgence in pertussis: elucidation of factors involved in the increased fitness of epidemic strains. PLoS One 2013;8(6):e66150.
41. Safarchi A, Octavia S, Luu LDW, Tay CY, Sintchenko V, Wood N, et al. Better colonisation of newly emerged Bordetella pertussis in the co-infection mouse model study. Vaccine 2016;34:3967-3971.
2. Advani A, Hallander HO, Dalby T, Krogfelt KA, Guiso N, Njamkepo E, et al. Pulsed-field gel electrophoresis analysis of Bordetella pertussis isolates circulating in Europe from 1998 to 2009. J Clin Microbiol 2013;51:422-428.
3. Winter K, Glaser C, Watt J, Harriman K, Centers for Disease Control and Prevention (CDC). Pertussis epidemic California, 2014. MMWR Morb Mortal Wkly Rep 2014;63:1129-1132.
4. Safarchi A, Octavia S, Wu SZ, Kaur S, Sintchenko V, Gilbert GL, et al. Genomic dissection of Australian Bordetella pertussis isolates from the 2008-2012 epidemic. J Infect 2016;72:468-477.
5. Sealey KL, Harris SR, Fry NK, Hurst LD, Gorringe AR, Parkhill J, et al. Genomic analysis of isolates from the United Kingdom 2012 pertussis outbreak reveals that vaccine antigen genes are unusually fast evolving. J Infect Dis 2015;212:294-301.
6. Cherry JD. Epidemic pertussis in 2012—the resurgence of a vaccine-preventable disease. N Engl J Med 2012;367:785-787.
7. Bart MJ, Harris SR, Advani A, Arakawa Y, Bottero D, Bouchez V, et al. Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. mBio 2014;5(2):e01074.
8. Bahmanjeh A, Noofeli M, Khaki P, Hassanzadeh SM. Genetic analysis of clinical and vaccine strains of Bordetella pertussis by pulsed-field gel electrophoresis (PFGE), multi locus sequence typing (MLST) and serotyping. Comp Immunol Microbiol Infect Dis 2019;64:168-175.
9. Dias W, van der Ark AA, Sakauchi MA, Kubrusly FS, Prestes AFR, Borges MM, et al. An improved whole cell pertussis vaccine with reduced content of endotoxin. Hum Vaccin Immunother 2013;9:339-348.
10. Moradi-Lakeh M, Esteghamati A. National immunization program in Iran: whys and why nots.Hum Vaccin Immunother 2013;9:112-114.
11. World Health Organization. WHO vaccine-preventable diseases: monitoring system 2013 global summary. 2013. Immunization schedule for. 2013;6.
12. Mooi FR. Bordetella pertussis and vaccination: the persistence of a genetically monomorphic pathogen. Infect Genet Evol 2010;10:36-49.
13. De Moissac Y, Ronald SL, Peppler MS. Use of pulsed-field gel electrophoresis for epidemiological study of Bordetella pertussis in a whooping cough outbreak. J Clin Microbiol 1994;32:398-402.
14. Bowden KE, Williams MM, Cassiday PK, Milton A, Pawloski L, Harrison M, et al. Molecular epidemiology of pertussis epidemic—Washington State, 2012. J Clin Microbiol 2014;52:3549-3557.
15. Weigand MR, Peng Y, Loparev V, Batra D, Bowden KE, Burroughs M, et al. The history of Bordetella pertussis genome evolution includes structural rearrangement. J Bacteriol 2017;199(8): e00806-00816.
16. Bart MJ, van Gent M, van der Heide HG, Boekhorst J, Hermans P, Parkhill J, et al. Comparative genomics of prevaccination and modern Bordetella pertussis strains. BMC Genomics 2010;11:627.
17. Belcher T, Preston A. Bordetella pertussis evolution in the (functional) genomics era. Pathog Dis 2015;73:ftv064.
18. Reischl U, Lehn N, Sanden GN, Loeffelholz MJ. Real-time PCR assay targeting IS481 of Bordetella pertussis and molecular basis for detecting Bordetella holmesii. J Clin Microbiol 2001;39:1963-1966.
19. Nikbin VS, Ahmadi NJ, Hosseinpour M, Lotfi MN, Shooraj F, Sadeghpour F, et al. Virulence factors variation among Bordetella pertussis isolates in Iran. Int J Mol Cell Med 2015;4:138-142.
20. Bottero D, Gaillard ME, Fingermann M, Weltman G, Fernández J, Sisti F, et al. Pulsed-field gel electrophoresis, pertactin, pertussis toxin S1 subunit polymorphisms, and surfaceome analysis of vaccine and clinical Bordetella pertussis strains. Clin Vaccine Immunol 2007;14:1490-1498.
21. Mooi FR, van Loo IH, Van Gent M, He Q, Bart MJ, Heuvelman KJ, et al. Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg Infect Dis 2009;15:1206-1213.
22. Haghighi F, Shahcheraghi F, Abbasi E, Eshraghi SS, Zeraati H, Mousavi SAJ, et al. Genetic profile variation in vaccine strains and clinical isolates of Bordetella pertussis recovered from Iranian patients. Avicenna J Med Biotechnol 2014;6:178-184.
23. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011;28:2731-2739.
24. Heravi FS, Nikbin VS, Lotfi MN, Badiri P, Ahmadi NJ, Zahraei SM, et al. Strain variation and antigenic divergence among Bordetella pertussis circulating strains isolated from patients in Iran. Eur J Clin Microbiol Infect Dis 2018;37:1893-1900.
25. Octavia S, Lan R. Frequent recombination and low level of clonality within Salmonella enterica subspecies I. Microbiology 2006;152:1099-1108.
26. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010;5(6):e11147.
27. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012;19:455-477.
28. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009;25:1754-1760.
29. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009;25:2078-2079.
30. Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, Harris DE, et al. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 2003;35:32-40.
31. Advani A, Donnelly D, Hallander H. Reference system for characterization of Bordetella pertussis pulsed-field gel electrophoresis profiles. J Clin Microbiol 2004;42:2890-2897.
32. Hallander H, Advani A, Riffelmann M, Von König CH, Caro V, Guiso N, et al. Bordetella pertussis strains circulating in Europe in 1999 to 2004 as determined by pulsed-field gel electrophoresis. J Clin Microbiol 2007;45:3257-3562.
33. Barkoff A-M, Mertsola J, Pierard D, Dalby T, Hoegh SV, Guillot S, et al. Surveillance of circulating Bordetella pertussis strains in Europe during 1998-2015. J Clin Microbiol 2018 Apr 25;56(5): e01998-02017.
34. Van Gent M, Heuvelman C, Van der Heide H, Hallander H, Advani A, Guiso N, et al. Analysis of Bordetella pertussis clinical isolates circulating in European countries during the period 1998–2012. Eur J Clin Microbiol Infect Dis 2015;34:821-830.
35. Shuel M, Jamieson FB, Tang P, Brown S, Farrell D, Martin I, et al. Genetic analysis of Bordetella pertussis in Ontario, Canada reveals one predominant clone. Int J Infect Dis 2013;17(6):e413-417.
36. Octavia S, Sintchenko V, Gilbert GL, Lawrence A, Keil AD, Hogg G, et al. Newly emerging clones of Bordetella pertussis carrying prn2 and ptxP3 alleles implicated in Australian pertussis epidemic in 2008–2010. J Infect Dis 2012;205:1220-1224.
37. Mosiej E, Augustynowicz E, Zawadka M, Dąbrowski W, Lutyńska A. Strain variation among Bordetella pertussis isolates circulating in Poland, after 50 years of whole-cell pertussis vaccine use. J Clin Microbiol 2011;49:1452-1457.
38. Polak M, Zasada AA, Mosiej E, Krysztopa-Grzybowska K, Witkowski L, Rzeczkowska M, et al. Pertactin-deficient Bordetella pertussis isolates in Poland—a country with whole-cell pertussis primary vaccination. Microbes Infect 2019;21:170-175.
39. de Gouw D, Hermans PW, Bootsma HJ, Zomer A, Heuvelman K, Diavatopoulos DA, et al. Differentially expressed genes in Bordetella pertussis strains belonging to a lineage which recently spread globally. PLoS One 2014;9(1):e84523.
40. King AJ, van der Lee S, Mohangoo A, van Gent M, van der Ark A, van de Waterbeemd B. Genome-wide gene expression analysis of Bordetella pertussis isolates associated with a resurgence in pertussis: elucidation of factors involved in the increased fitness of epidemic strains. PLoS One 2013;8(6):e66150.
41. Safarchi A, Octavia S, Luu LDW, Tay CY, Sintchenko V, Wood N, et al. Better colonisation of newly emerged Bordetella pertussis in the co-infection mouse model study. Vaccine 2016;34:3967-3971.
| Files | ||
| Issue | Vol 12 No 1 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i1.2500 | |
| Keywords | ||
| Bordetella pertussis Genome diversity Pulsed-field gel electrophoresis Whole genome sequencing | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Saedi S, Safarchi A, Noofeli M, Tadayon K, Chin Yen Tay A, Lamichhane B, Rahimi H, Shahcheraghi F. Genome diversity and evolutionary characteristics of clinical isolates of Bordetella pertussis circulating in Iran. Iran J Microbiol. 2020;12(1):1-10.
