Pilus operon evolution in Streptococcus pneumoniae is driven by positive selection and recombination

PLoS ONE

Volumn 3, Issue 11, 2008, Pages

  Muzzi, Alessandro ^a   Moschioni, Monica ^a   Covacci, Antonello ^a   Rappuoli, Rino ^a   Donati, Claudio ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; SORTASE; AMINOACYLTRANSFERASE; CYSTEINE PROTEINASE; RLRA PROTEIN, STREPTOCOCCUS PNEUMONIAE; SORTASE B; SORTASE C; SORTASE D; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM ISOLATE; BACTERIUM PILUS; CELL ADHESION; CELL ORGANELLE; CHROMOSOME MOSAICISM; DISEASE MODEL; EPITHELIUM CELL; GENETIC CONSERVATION; GENETIC RECOMBINATION; GENETIC SELECTION; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; IN VITRO STUDY; LUNG ALVEOLUS EPITHELIUM; MULTILOCUS SEQUENCE TYPING; NONHUMAN; OPERON; STREPTOCOCCUS PNEUMONIAE; BACTERIUM ADHERENCE; DNA SEQUENCE; FIMBRIA; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); MURINAE; STREPTOCOCCUS PNEUMONIAE;

AMINOACYLTRANSFERASES; BACTERIAL ADHESION; BACTERIAL PROTEINS; BASE SEQUENCE; CYSTEINE ENDOPEPTIDASES; EVOLUTION, MOLECULAR; FIMBRIAE, BACTERIAL; MOLECULAR SEQUENCE DATA; OPERON; RECOMBINATION, GENETIC; SELECTION (GENETICS); SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; STREPTOCOCCUS PNEUMONIAE; TRANS-ACTIVATORS;

EID: 56349122122     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003660     Document Type: Article

References (45)

1. Barocchi MA, Ries J, Zogaj X, Hemsley C, Albiger B, et al. (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proc Natl Acad Sci U S A 103: 2857-2862.
2. Nelson AL, Ries J, Bagnoli F, Dahlberg S, Falker S, et al. (2007) RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol Microbiol 66: 329-340.
3. Gianfaldoni C, Censini S, Hilleringmann M, Moschioni M, Facciotti C, et al. (2007) Streptococcus pneumoniae pilus subunits protect mice against lethal challenge. Infect Immun 75: 1059-1062.
4. Hilleringmann M, Giusti F, Baudner BC, Masignani V, Covacci A, et al. (2008) Pneumococcal Pili Are Composed of Protofilaments Exposing Adhesive Clusters of Rrg A. PLoS Pathogens 4.
5. LeMieux J, Hava DL, Basset A, Camilli A (2006) RrgA and RrgB are components of a multisubunit pilus encoded by the Streptococcus pneumoniae rlrA pathogenicity islet. Infect Immun 74: 2453-2456.
6. Moschioni M, Donati C, Muzzi A, Masignani V, Censini S, et al. (2008) Streptococcus pneumoniae Contains 3 rlrA Pilus Variants That Are Clonally Related. J Infect Dis.
7. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG (2004) eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186: 1518-1530.
8. Bagnoli F, Moschioni M, Donati C, Dimitrovska V, Ferlenghi I, et al. (2008) A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J Bacteriol 190: 5480-5492.
9. Telford JL, Barocchi MA, Margarit I, Rappuoli R, Grandi G (2006) Pili in gram-positive pathogens. Nat Rev Microbiol 4: 509-519.
10. Claverys JP, Prudhomme M, Mortier-Barriere I, Martin B (2000) Adaptation to the environment: Streptococcus pneumoniae, a paradigm for recombination-mediated genetic plasticity? Mol Microbiol 35: 251-259.
11. Feil EJ, Holmes EC, Bessen DE, Chan MS, Day NP, et al. (2001) Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc Natl Acad Sci U S A 98: 182-187.
12. McVean GA, Myers SR, Hunt S, Deloukas P, Bentley DR, et al. (2004) The fine-scale structure of recombination rate variation in the human genome. Science 304: 581-584.
13. Fearnhead P (2006) SequenceLDhot: detecting recombination hotspots. Bioinformatics 22: 3061-3066.
14. Stumpf MP, McVean GA (2003) Estimating recombination rates from population-genetic data. Nat Rev Genet 4: 959-968.
15. Smith NH, Maynard Smith J, Spratt BG (1995) Sequence evolution of the porB gene of Neisseria gonorrhoeae and Neisseria meningitidis: evidence of positive Darwinian selection. Mol Biol Evol 12: 363-370.
16. Boyd EF, Hartl DL (1998) Diversifying selection governs sequence polymorphism in the major adhesin proteins fimA, papA, and sfaA of Escherichia coli. J Mol Evol 47: 258-267.
17. McGraw EA, Li J, Selander RK, Whittam TS (1999) Molecular evolution and mosaic structure of alpha, beta, and gamma intimins of pathogenic Escherichia coli. Mol Biol Evol 16: 12-22.
18. Polley SD, Conway DJ (2001) Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 158: 1505-1512.
19. Baum J, Thomas AW, Conway DJ (2003) Evidence for diversifying selection on erythrocyte-binding antigens of Plasmodium falciparum and P. vivax. Genetics 163: 1327-1336.
20. Wang L, Rothemund D, Curd H, Reeves PR (2003) Species-wide variation in the Escherichia coli flagellin (H-antigen) gene. J Bacteriol 185: 2936-2943.
21. Kalia A, Bessen DE (2004) Natural selection and evolution of streptococcal virulence genes involved in tissue-specific adaptations. J Bacteriol 186: 110-121.
22. Guttman DS, Gropp SJ, Morgan RL, Wang PW (2006) Diversifying selection drives the evolution of the type III secretion system pilus of Pseudomonas syringae. Mol Biol Evol 23: 2342-2354.
23. Urwin R, Holmes EC, Fox AJ, Derrick JP, Maiden MC (2002) Phylogenetic evidence for frequent positive selection and recombination in the meningococcal surface antigen PorB. Mol Biol Evol 19: 1686-1694.
24. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
25. Yang Z, Nielsen R (2002) Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19: 908-917.
26. Yang Z, Wong WS, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107-1118.
27. Anisimova M, Nielsen R, Yang Z (2003) Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164: 1229-1236.
28. Wilson DJ, McVean G (2006) Estimating diversifying selection and functional constraint in the presence of recombination. Genetics 172: 1411-1425.
29. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
30. Hudson RR (2001) Two-locus sampling distributions and their application. Genetics 159: 1805-1817.
31. Fraser C, Hanage WP, Spratt BG (2007) Recombination and the nature of bacterial speciation. Science 315: 476-480.
32. Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21: 260-262.
33. Wildschutte H, Wolfe DM, Tamewitz A, Lawrence JG (2004) Protozoan predation, diversifying selection, and the evolution of antigenic diversity in Salmonella. Proc Natl Acad Sci U S A 101: 10644-10649.
34. Lipsitch M, O'Hagan JJ (2007) Patterns of antigenic diversity and the mechanisms that maintain them. J R Soc Interface 4: 787-802.
35. Cooper TF (2007) Recombination Speeds Adaptation by Reducing Competition between Beneficial Mutations in Populations of Escherichia coli. PLoS Biol 5: e225.
36. Brueggemann AB, Pai R, Crook DW, Beall B (2007) Vaccine Escape Recombinants Emerge after Pneumococcal Vaccination in the United States. PLoS Pathogens 3: e168.
37. 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.
38. Enright MC, Spratt BG (1998) A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology 144 (Pt 11): 3049-3060.
39. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205-217.
40. Lynch M, Crease TJ (1990) The analysis of population survey data on DNA sequence variation. Mol Biol Evol 7: 377-394.
41. Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7: 256-276.
42. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
43. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
44. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101: 11030-11035.
45. Fearnhead P, Donnelly P (2001) Estimating recombination rates from population genetic data. Genetics 159: 1299-1318.