Heterogeneity in the Frequency and Characteristics of Homologous Recombination in Pneumococcal Evolution

English version České info

Streptococcus pneumoniae, a bacterium commonly carried asymptomatically by children, is a major cause of diseases such as pneumonia and meningitis. The species is genetically diverse and is known to frequently undergo the remarkable process of transformation via homologous recombination. In this process, the bacterial cell incorporates DNA from other, closely related bacteria into its own genome, which can result in the development of antibiotic resistance or allow cells to evade vaccines. Therefore it is important to quantify the impact of this process on the evolution of S. pneumoniae to understand how quickly the species can respond to the introduction of such clinical interventions. In this study we followed the recombination process by studying the evolution of two important and very different lineages of S. pneumoniae, PMEN1 and CC180, using newly available population genomic data. We found that pneumococcus evolves via two distinct processes that we term micro- and macro-recombination. Micro-recombination led to acquisition of single, short DNA fragments, while macro-recombination tended to incorporate multiple, long DNA fragments. Interestingly, macro-recombination was associated with major phenotypic changes. We argue that greater insight into the adaptive role of recombination in pneumococcus requires a good understanding of both rates of homologous recombination and population dynamics of the bacterium in natural populations.

Vyšlo v časopise: Heterogeneity in the Frequency and Characteristics of Homologous Recombination in Pneumococcal Evolution. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004300
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004300

Souhrn

Zdroje

1. GriffithF (1928) The Significance of Pneumococcal Types. J Hyg (Lond) 27: 113–159.

2. CoffeyTJ, DowsonCG, DanielsM, ZhouJ, MartinC, et al. (1991) Horizontal transfer of multiple penicillin-binding protein genes, and capsular biosynthetic genes, in natural populations of Streptococcus pneumoniae. Mol Microbiol 5: 2255–2260.

3. SmithJM, SmithNH, O'RourkeM, SprattBG (1993) How clonal are bacteria? Proc Natl Acad Sci USA 90: 4384–4388.

4. FeilEJ, SmithJM, EnrightMC, SprattBG (2000) Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics 154: 1439–1450.

5. ClaverysJP, LefevreJC, SicardAM (1980) Transformation of Streptococcus pneumoniae with S. pneumoniae-lambda phage hybrid DNA: induction of deletions. Proc Natl Acad Sci USA 77: 3534–3538.

6. PolzMF, AlmEJ, HanageWP (2013) Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet 29: 170–175.

7. PrudhommeM, LibanteV, ClaverysJP (2002) Homologous recombination at the border: insertion-deletions and the trapping of foreign DNA in Streptococcus pneumoniae. Proc Natl Acad Sci USA 99: 2100–2105.

8. DowsonCG, HutchisonA, BranniganJA, GeorgeRC, HansmanD, et al. (1989) Horizontal transfer of penicillin-binding protein genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Proc Natl Acad Sci USA 86: 8842–8846.

9. LipsitchM (1999) Bacterial vaccines and serotype replacement: lessons from Haemophilus influenzae and prospects for Streptococcus pneumoniae. Emerging Infect Dis 5: 336–345.

10. SprattBG, GreenwoodBM (2000) Prevention of pneumococcal disease by vaccination: does serotype replacement matter? Lancet 356: 1210–1211.

11. HanageWP, FraserC, TangJ, ConnorTR, CoranderJ (2009) Hyper-recombination, diversity, and antibiotic resistance in pneumococcus. Science 324: 1454–1457.

12. CroucherNJ, FinkelsteinJA, PeltonSI, MitchellPK, LeeGM, et al. (2013) Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat Genet 45: 656–663.

13. CroucherNJ, HarrisSR, BarquistL, ParkhillJ, BentleySD (2012) A high-resolution view of genome-wide pneumococcal transformation. PLoS Pathog 8: e1002745.

14. HillerNL, AhmedA, PowellE, MartinDP, EutseyR, et al. (2010) Generation of genic diversity among Streptococcus pneumoniae strains via horizontal gene transfer during a chronic polyclonal pediatric infection. PLoS Pathog 6: e1001108.

15. GolubchikT, BrueggemannAB, StreetT, GertzRE, SpencerCC, et al. (2012) Pneumococcal genome sequencing tracks a vaccine escape variant formed through a multi-fragment recombination event. Nat Genet 44: 352–355.

16. WyresKL, LambertsenLM, CroucherNJ, McGeeL, von GottbergA, et al. (2012) The multidrug-resistant PMEN1 pneumococcus is a paradigm for genetic success. Genome Biol 13: R103.

17. HsiehYC, WangJT, LeeWS, HsuehPR, ShaoPL, et al. (2006) Serotype competence and penicillin resistance in Streptococcus pneumoniae. Emerging Infect Dis 12: 1709–1714.

18. EvansBA, RozenDE (2013) Significant variation in transformation frequency in Streptococcus pneumoniae. ISME J 7: 791–799.

19. CroucherNJ, HarrisSR, FraserC, QuailMA, BurtonJ, et al. (2011) Rapid pneumococcal evolution in response to clinical interventions. Science 331: 430–434.

20. CroucherNJ, MitchellAM, GouldKA, InverarityD, BarquistL, et al. (2013) Dominant role of nucleotide substitution in the diversification of serotype 3 pneumococci over decades and during a single infection. PLoS Genet 9: e1003868.

21. DidelotX, FalushD (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175: 1251–1266.

22. CroucherNJ, WalkerD, RomeroP, LennardN, PatersonGK, et al. (2009) Role of conjugative elements in the evolution of the multidrug-resistant pandemic clone Streptococcus pneumoniaeSpain23F ST81. J Bacteriol 191: 1480–1489.

23. HumbertO, PrudhommeM, HakenbeckR, DowsonCG, ClaverysJP (1995) Homeologous recombination and mismatch repair during transformation in Streptococcus pneumoniae: saturation of the Hex mismatch repair system. Proc Natl Acad Sci USA 92: 9052–9056.

24. MajewskiJ, ZawadzkiP, PickerillP, CohanFM, DowsonCG (2000) Barriers to genetic exchange between bacterial species: Streptococcus pneumoniae transformation. J Bacteriol 182: 1016–1023.

25. HarrisSR, FeilEJ, HoldenMT, QuailMA, NickersonEK, et al. (2010) Evolution of MRSA during hospital transmission and intercontinental spread. Science 327: 469–474.

26. BrochetM, RusniokC, CouveE, DramsiS, PoyartC, et al. (2008) Shaping a bacterial genome by large chromosomal replacements, the evolutionary history of Streptococcus agalactiae. Proc Natl Acad Sci USA 105: 15961–15966.

27. AttaiechL, OlivierA, Mortier-BarriereI, SouletAL, GranadelC, et al. (2011) Role of the single-stranded DNA-binding protein SsbB in pneumococcal transformation: maintenance of a reservoir for genetic plasticity. PLoS Genet 7: e1002156.

28. BlackLW (1989) DNA packaging in dsDNA bacteriophages. Annu Rev Microbiol 43: 267–292.

29. MoscosoM, GarciaE, LopezR (2006) Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J Bacteriol 188: 7785–7795.

30. VosM (2009) Why do bacteria engage in homologous recombination? Trends Microbiol 17: 226–232.