Selective and Genetic Constraints on Pneumococcal Serotype Switching

PLoS Genetics

Volumn 11, Issue 3, 2015, Pages

  Croucher, Nicholas J ^a,b   Kagedan, Lisa ^b   Thompson, Claudette M ^b   Parkhill, Julian ^c   Bentley, Stephen D ^c   Finkelstein, Jonathan A ^d,e   Lipsitch, Marc ^b   Hanage, William P ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d HARVARD MEDICAL SCHOOL   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PENICILLIN BINDING PROTEIN 2X; ANTIBODY; PNEUMOCOCCUS VACCINE;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL METABOLISM; BACTERIAL STRAIN; CONTROLLED STUDY; EPISTASIS; GENE IDENTIFICATION; GENE INTERACTION; GENE LOCUS; GENE REARRANGEMENT; GENE SWITCHING; GENETIC LINKAGE; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOME ANALYSIS; GENOTYPE; NONHUMAN; PBP1A GENE; PBP2X GENE; PHENOTYPE; PHYLOGENY; SEQUENCE ANALYSIS; SEROTYPE; STREPTOCOCCUS PNEUMONIAE; WZY GENE; ANTIBIOTIC RESISTANCE; GENETICS; HOMOLOGOUS RECOMBINATION; HUMAN; IMMUNOLOGY; MICROBIOLOGY; PATHOGENICITY; PNEUMOCOCCAL INFECTION; SEQUENCE ALIGNMENT; SEROTYPING;

STREPTOCOCCUS PNEUMONIAE;

ANTIBODIES; BETA-LACTAM RESISTANCE; GENOME, BACTERIAL; GENOTYPE; HOMOLOGOUS RECOMBINATION; HUMANS; PHYLOGENY; PNEUMOCOCCAL INFECTIONS; PNEUMOCOCCAL VACCINES; SEQUENCE ALIGNMENT; SEROGROUP; SEROTYPING; STREPTOCOCCUS PNEUMONIAE;

EID: 84926308364     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005095     Document Type: Article

References (49)

1. Kadioglu A, Weiser JN, Paton JC, Andrew PW, (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6: 288–301. doi: 10.1038/nrmicro1871 18340341
2. Bentley SD, Aanensen DM, Mavroidi A, Saunders D, Rabbinowitsch E, et al. (2006) Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2: e31. 16532061
3. Park IH, Park S, Hollingshead SK, Nahm MH, (2007) Genetic basis for the new pneumococcal serotype, 6C. Infect Immun 75: 4482–4489. 17576753
4. Calix JJ, Nahm MH, (2010) A new pneumococcal serotype, 11E, has a variably inactivated wcjE gene. Journal of Infectious Diseases 202: 29–38. doi: 10.1086/653123 20507232
5. Calix JJ, Porambo RJ, Brady AM, Larson TR, Yother J, et al. (2012) Biochemical, Genetic, and Serological Characterization of Two Capsule Subtypes among Streptococcus pneumoniae Serotype 20 Strains. Journal of Biological Chemistry 287: 27885–27894. doi: 10.1074/jbc.M112.380451 22736767
6. Salter SJ, Hinds J, Gould KA, Lambertsen L, Hanage WP, et al. (2012) Variation at the capsule locus, cps, of mistyped and non-typable Streptococcus pneumoniae isolates. Microbiology 158: 1560–1569. doi: 10.1099/mic.0.056580-0 22403189
7. Bratcher PE, Kim KH, Kang JH, Hong JY, Nahm MH, (2010) Identification of natural pneumococcal isolates expressing serotype 6D by genetic, biochemical and serological characterization. Microbiology 156: 555–560. doi: 10.1099/mic.0.034116-0 19942663
8. Hyams C, Camberlein E, Cohen JM, Bax K, Brown JS, (2010) The Streptococcus pneumoniae capsule inhibits complement activity and neutrophil phagocytosis by multiple mechanisms. Infect Immun 78: 704–715. doi: 10.1128/IAI.00881-09 19948837
9. Lipsitch M, Whitney CG, Zell E, Kaijalainen T, Dagan R, et al. (2005) Are anticapsular antibodies the primary mechanism of protection against invasive pneumococcal disease? PLoS medicine 2: e15. 15696204
10. Weinberger DM, Dagan R, Givon-Lavi N, Regev-Yochay G, Malley R, et al. (2008) Epidemiologic evidence for serotype-specific acquired immunity to pneumococcal carriage. J Infect Dis 197: 1511–1518. doi: 10.1086/587941 18471062
11. Hill PC, Cheung YB, Akisanya A, Sankareh K, Lahai G, et al. (2008) Nasopharyngeal carriage of Streptococcus pneumoniae in Gambian infants: a longitudinal study. Clin Infect Dis 46: 807–814. doi: 10.1086/528688 18279039
12. Goldblatt D, Hussain M, Andrews N, Ashton L, Virta C, et al. (2005) Antibody responses to nasopharyngeal carriage of Streptococcus pneumoniae in adults: a longitudinal household study. Journal of Infectious Diseases 192: 387–393. 15995951
13. Cobey S, Lipsitch M, (2012) Niche and neutral effects of acquired immunity permit coexistence of pneumococcal serotypes. Science 335: 1376–1380. doi: 10.1126/science.1215947 22383809
14. Ghaffar F, Barton T, Lozano J, Muniz LS, Hicks P, et al. (2004) Effect of the 7-valent pneumococcal conjugate vaccine on nasopharyngeal colonization by Streptococcus pneumoniae in the first 2 years of life. Clinical Infectious Diseases 39: 930–938. 15472842
15. Rinta-Kokko H, Dagan R, Givon-Lavi N, Auranen K, (2009) Estimation of vaccine efficacy against acquisition of pneumococcal carriage. Vaccine 27: 3831–3837. doi: 10.1016/j.vaccine.2009.04.009 19490983
16. Huang SS, Hinrichsen VL, Stevenson AE, Rifas-Shiman SL, Kleinman K, et al. (2009) Continued impact of pneumococcal conjugate vaccine on carriage in young children. Pediatrics 124: e1–11. doi: 10.1542/peds.2008-3099 19564254
17. Millar EV, O'Brien KL, Watt JP, Bronsdon MA, Dallas J, et al. (2006) Effect of community-wide conjugate pneumococcal vaccine use in infancy on nasopharyngeal carriage through 3 years of age: a cross-sectional study in a high-risk population. Clin Infect Dis 43: 8–15. 16758412
18. Lipsitch M, (1997) Vaccination against colonizing bacteria with multiple serotypes. Proc Natl Acad Sci U S A 94: 6571–6576. 9177259
19. Lipsitch M, (1999) Bacterial vaccines and serotype replacement: lessons from Haemophilus influenzae and prospects for Streptococcus pneumoniae. Emerg Infect Dis 5: 336–345. 10341170
20. Spratt BG, Greenwood BM, (2000) Prevention of pneumococcal disease by vaccination: does serotype replacement matter? Lancet 356: 1210–1211. 11072934
21. Hanage WP, Bishop CJ, Huang SS, Stevenson AE, Pelton SI, et al. (2011) Carried pneumococci in Massachusetts children: the contribution of clonal expansion and serotype switching. Pediatr Infect Dis J 30: 302–308. doi: 10.1097/INF.0b013e318201a154 21085049
22. Robinson KA, Baughman W, Rothrock G, Barrett NL, Pass M, et al. (2001) Epidemiology of invasive Streptococcus pneumoniae infections in the United States, 1995–1998: Opportunities for prevention in the conjugate vaccine era. JAMA 285: 1729–1735. 11277827
23. Hanage WP, Finkelstein JA, Huang SS, Pelton SI, Stevenson AE, et al. (2010) Evidence that pneumococcal serotype replacement in Massachusetts following conjugate vaccination is now complete. Epidemics 2: 80–84. doi: 10.1016/j.epidem.2010.03.005 21031138
24. Black S, Shinefield H, Fireman B, Lewis E, Ray P, et al. (2000) Efficacy, safety and immunogenicity of heptavalent pneumococcal conjugate vaccine in children. Northern California Kaiser Permanente Vaccine Study Center Group. Pediatr Infect Dis J 19: 187–195. 10749457
25. Croucher NJ, Finkelstein JA, Pelton SI, Mitchell PK, Lee GM, et al. (2013) Population genomics of post-vaccine changes in pneumococcal epidemiology. Nature genetics 45: 656–663. doi: 10.1038/ng.2625 23644493
26. Wyres KL, Lambertsen LM, Croucher NJ, McGee L, von Gottberg A, et al. (2013) Pneumococcal Capsular Switching: A Historical Perspective. Journal of Infectious Diseases 207: 439–449. doi: 10.1093/infdis/jis703 23175765
27. Feil EJ, Smith JM, Enright MC, Spratt BG, (2000) Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics 154: 1439–1450. 10747043
28. Croucher NJ, Harris SR, Barquist L, Parkhill J, Bentley SD, (2012) A high-resolution view of genome-wide pneumococcal transformation. PLoS Pathog 8: e1002745. doi: 10.1371/journal.ppat.1002745 22719250
29. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, et al. (2011) Rapid pneumococcal evolution in response to clinical interventions. Science 331: 430–434. doi: 10.1126/science.1198545 21273480
30. Croucher NJ, Hanage WP, Harris SR, McGee L, van der Linden M, et al. (2014) Variable recombination dynamics during the emergence, transmission and 'disarming' of a multidrug-resistant pneumococcal clone. BMC biology 12: 49. doi: 10.1186/1741-7007-12-49 24957517
31. Hausdorff WP, Feikin DR, Klugman KP, (2005) Epidemiological differences among pneumococcal serotypes. The Lancet Infectious Diseases 5: 83–93. 15680778
32. Trzcinski K, Thompson CM, Lipsitch M, (2004) Single-step capsular transformation and acquisition of penicillin resistance in Streptococcus pneumoniae. J Bacteriol 186: 3447–3452. 15150231
33. Croucher NJ, Chewapreecha C, Hanage WP, Harris SR, McGee L, et al. (2014) Evidence for soft selective sweeps in the evolution of pneumococcal multidrug resistance and vaccine escape. Genome Biology and Evolution 6: 1589–1602. doi: 10.1093/gbe/evu120 24916661
34. Gupta S, Maiden MC, Feavers IM, Nee S, May RM, et al. (1996) The maintenance of strain structure in populations of recombining infectious agents. Nature medicine 2: 437–442. 8597954
35. Mavroidi A, Aanensen DM, Godoy D, Skovsted IC, Kaltoft MS, et al. (2007) Genetic relatedness of the Streptococcus pneumoniae capsular biosynthetic loci. Journal of bacteriology 189: 7841–7855. 17766424
36. Mostowy R, Croucher NJ, Hanage WP, Harris SR, Bentley S, et al. (2014) Heterogeneity in the Frequency and Characteristics of Homologous Recombination in Pneumococcal Evolution. PLOS Genetics 10: e1004300. doi: 10.1371/journal.pgen.1004300 24786281
37. Weinberger DM, Trzcinski K, Lu YJ, Bogaert D, Brandes A, et al. (2009) Pneumococcal capsular polysaccharide structure predicts serotype prevalence. PLoS Pathog 5: e1000476. doi: 10.1371/journal.ppat.1000476 19521509
38. Bidossi A, Mulas L, Decorosi F, Colomba L, Ricci S, et al. (2012) A functional genomics approach to establish the complement of carbohydrate transporters in Streptococcus pneumoniae. PLoS One 7: e33320. doi: 10.1371/journal.pone.0033320 22428019
39. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, et al. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498–506. 11463916
40. Kryazhimskiy S, Dushoff J, Bazykin GA, Plotkin JB, (2011) Prevalence of epistasis in the evolution of influenza A surface proteins. PLOS Genetics 7: e1001301. doi: 10.1371/journal.pgen.1001301 21390205
41. Croucher NJ, Coupland PG, Stevenson AE, Callendrello A, Bentley SD, et al. (2014) Diversification of bacterial genome content through distinct mechanisms over different timescales. Nature communications 5:5471. doi: 10.1038/ncomms6471 25407023
42. Humbert O, Prudhomme M, Hakenbeck R, Dowson CG, Claverys J-P, (1995) Homeologous recombination and mismatch repair during transformation in Streptococcus pneumoniae: saturation of the Hex mismatch repair system. Proceedings of the National Academy of Sciences 92: 9052–9056. 7568071
43. Chewapreecha C, Harris SR, Croucher NJ, Turner C, Marttinen P, et al. (2014) Dense genomic sampling identifies highways of pneumococcal recombination. Nature genetics 46: 305–309. doi: 10.1038/ng.2895 24509479
44. Johnston C, Martin B, Granadel C, Polard P, Claverys J-P, (2013) Programmed protection of foreign DNA from restriction allows pathogenicity island exchange during pneumococcal transformation. PLoS pathogens 9: e1003178. doi: 10.1371/journal.ppat.1003178 23459610
45. Hathaway LJ, Brugger SD, Morand B, Bangert M, Rotzetter JU, et al. (2012) Capsule type of Streptococcus pneumoniae determines growth phenotype. PLoS pathogens 8: e1002574. doi: 10.1371/journal.ppat.1002574 22412375
46. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, et al. (2014) Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic acids research: gku1196.
47. Paradis E, Claude J, Strimmer K, (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290. 14734327
48. Sung C, Li H, Claverys J, Morrison D, (2001) An rpsL cassette, Janus, for gene replacement through negative selection in Streptococcus pneumoniae. Applied and environmental microbiology 67: 5190–5196. 11679344
49. Trzcinski K, Thompson CM, Lipsitch M, (2003) Construction of otherwise isogenic serotype 6B, 7F, 14, and 19F capsular variants of Streptococcus pneumoniae strain TIGR4. Applied and environmental microbiology 69: 7364–7370. 14660386