A variable region within the genome of streptococcus pneumoniae contributes to strain-strain variation in virulence

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Harvey, Richard M ^a   Stroeher, Uwe H ^a,c   Ogunniyi, Abiodun D ^a   Smith Vaughan, Heidi C ^b   Leach, Amanda J ^b   Paton, James C ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b MENZIES SCHOOL OF HEALTH RESEARCH   (Australia)

^c FLINDERS UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL ENDOCARDITIS; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE LOCUS; GENE SEQUENCE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SEROTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; STREPTOCOCCUS PNEUMONIAE; ANIMAL; BACTERIAL COUNT; BACTERIAL GENE; BAGG ALBINO MOUSE; CLASSIFICATION; DISEASE MODEL; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; GENOMIC ISLAND; HUMAN; ISOLATION AND PURIFICATION; LUNG; MICROBIOLOGY; MUTATION; NASOPHARYNX; PATHOGENICITY; PHENOTYPE; PNEUMOCOCCAL INFECTION; REPRODUCIBILITY; SEROTYPING; SPECIES DIFFERENCE; VIRULENCE;

BACTERIA (MICROORGANISMS); MURINAE; MUS; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; COLONY COUNT, MICROBIAL; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENETIC VARIATION; GENOME, BACTERIAL; GENOMIC ISLANDS; HUMANS; LUNG; MICE; MICE, INBRED BALB C; MUTATION; NASOPHARYNX; PHENOTYPE; PNEUMOCOCCAL INFECTIONS; REPRODUCIBILITY OF RESULTS; SEQUENCE ANALYSIS, DNA; SEROTYPING; SPECIES SPECIFICITY; STREPTOCOCCUS PNEUMONIAE; VIRULENCE;

EID: 79955848787     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019650     Document Type: Article

References (83)

1. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, et al. (2009) Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374: 893-902.
2. Brueggemann AB, Griffiths DT, Meats E, Peto T, Crook DW, et al. (2003) Clonal relationships between invasive and carriage Streptococcus pneumoniae and serotype- and clone-specific differences in invasive disease potential. J Infect Dis 187: 1424-1432.
3. Brueggemann AB, Peto TE, Crook DW, Butler JC, Kristinsson KG, et al. (2004) Temporal and geographic stability of the serogroup-specific invasive disease potential of Streptococcus pneumoniae in children. J Infect Dis 190: 1203-1211.
4. Sandgren A, Albiger B, Orihuela CJ, Tuomanen E, Normark S, et al. (2005) Virulence in mice of pneumococcal clonal types with known invasive disease potential in humans. J Infect Dis 192: 791-800.
5. Sandgren A, Sjostrom K, Olsson-Liljequist B, Christensson B, Samuelsson A, et al. (2004) Effect of clonal and serotype-specific properties on the invasive capacity of Streptococcus pneumoniae. J Infect Dis 189: 785-796.
6. Sjostrom K, Spindler C, Ortqvist A, Kalin M, Sandgren A, et al. (2006) Clonal and capsular types decide whether pneumococci will act as a primary or opportunistic pathogen. Clin Infect Dis 42: 451-459.
7. Nunes S, Sa-Leao R, Pereira LC, Lencastre H, (2008) Emergence of a serotype 1 Streptococcus pneumoniae lineage colonising healthy children in Portugal in the seven-valent conjugate vaccination era. Clin Microbiol Infect 14: 82-84.
8. Smith-Vaughan H, Marsh R, Mackenzie G, Fisher J, Morris PS, et al. (2009) Age-specific cluster of cases of serotype 1 Streptococcus pneumoniae carriage in remote indigenous communities in Australia. Clin Vaccine Immunol 16: 218-221.
9. Silva NA, McCluskey J, Jefferies JM, Hinds J, Smith A, et al. (2006) Genomic diversity between strains of the same serotype and multilocus sequence type among pneumococcal clinical isolates. Infect Immun 74: 3513-3518.
10. Obert C, Sublett J, Kaushal D, Hinojosa E, Barton T, et al. (2006) Identification of a Candidate Streptococcus pneumoniae core genome and regions of diversity correlated with invasive pneumococcal disease. Infect Immun 74: 4766-4777.
11. 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.
12. Hiller NL, Janto B, Hogg JS, Boissy R, Yu S, et al. (2007) Comparative genomic analyses of seventeen Streptococcus pneumoniae strains: insights into the pneumococcal supragenome. J Bacteriol 189: 8186-8195.
13. Bruckner R, Nuhn M, Reichmann P, Weber B, Hakenbeck R, (2004) Mosaic genes and mosaic chromosomes-genomic variation in Streptococcus pneumoniae. Int J Med Microbiol 294: 157-168.
14. Blomberg C, Dagerhamn J, Dahlberg S, Browall S, Fernebro J, et al. (2009) Pattern of accessory regions and invasive disease potential in Streptococcus pneumoniae. J Infect Dis 199: 1032-1042.
15. Aguiar SI, Serrano I, Pinto FR, Melo-Cristino J, Ramirez M, (2008) The presence of the pilus locus is a clonal property among pneumococcal invasive isolates. BMC Microbiol 8: 41.
16. 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.
17. Basset A, Trzcinski K, Hermos C, O'Brien KL, Reid R, et al. (2007) Association of the pneumococcal pilus with certain capsular serotypes but not with increased virulence. J Clin Microbiol 45: 1684-1689.
18. Orihuela CJ, (2009) Role played by psrP-secY2A2 (accessory region 34) in the invasive disease potential of Streptococcus pneumoniae. J Infect Dis 200: 1180-1181; author reply 1181-1182.
19. Shivshankar P, Sanchez C, Rose LF, Orihuela CJ, (2009) The Streptococcus pneumoniae adhesin PsrP binds to Keratin 10 on lung cells. Mol Microbiol 73: 663-679.
20. Sjostrom K, Blomberg C, Fernebro J, Dagerhamn J, Morfeldt E, et al. (2007) Clonal success of piliated penicillin nonsusceptible pneumococci. Proc Natl Acad Sci U S A 104: 12907-12912.
21. Sanchez CJ, Shivshankar P, Stol K, Trakhtenbroit S, Sullam PM, et al. (2010) The pneumococcal serine-rich repeat protein is an intra-species bacterial adhesin that promotes bacterial aggregation in vivo and in biofilms. PLoS Pathog 6.
22. Hyams C, Yuste J, Bax K, Camberlein E, Weiser JN, et al. (2010) Streptococcus pneumoniae resistance to complement-mediated immunity is dependent on the capsular serotype. Infect Immun 78: 716-725.
23. Weinberger DM, Trzcinski K, Lu YJ, Bogaert D, Brandes A, et al. (2009) Pneumococcal capsular polysaccharide structure predicts serotype prevalence. PLoS Pathog 5: e1000476.
24. Melin M, Trzcinski K, Antonio M, Meri S, Adegbola R, et al. (2010) Serotype related variation in susceptibility to complement deposition and opsonophagocytosis among clinical isolates of Streptococcus pneumoniae. Infect Immun.
25. Melin M, Trzcinski K, Meri S, Kayhty H, Vakevainen M, (2010) The capsular serotype of Streptococcus pneumoniae is more important than the genetic background for resistance to complement. Infect Immun.
26. Brueggemann AB, Spratt BG, (2003) Geographic distribution and clonal diversity of Streptococcus pneumoniae serotype 1 isolates. J Clin Microbiol 41: 4966-4970.
27. Antonio M, Hakeem I, Awine T, Secka O, Sankareh K, et al. (2008) Seasonality and outbreak of a predominant Streptococcus pneumoniae serotype 1 clone from The Gambia: expansion of ST217 hypervirulent clonal complex in West Africa. BMC Microbiol 8: 198.
28. Leimkugel J, Adams Forgor A, Gagneux S, Pfluger V, Flierl C, et al. (2005) An outbreak of serotype 1 Streptococcus pneumoniae meningitis in northern Ghana with features that are characteristic of Neisseria meningitidis meningitis epidemics. J Infect Dis 192: 192-199.
29. Yaro S, Lourd M, Traore Y, Njanpop-Lafourcade BM, Sawadogo A, et al. (2006) Epidemiological and molecular characteristics of a highly lethal pneumococcal meningitis epidemic in Burkina Faso. Clin Infect Dis 43: 693-700.
30. van der Ploeg JR, (2010) Genome sequence of the temperate bacteriophage PH10 from Streptococcus oralis. Virus Genes.
31. Romero P, Croucher NJ, Hiller NL, Hu FZ, Ehrlich GD, et al. (2009) Comparative genomic analysis of ten Streptococcus pneumoniae temperate bacteriophages. J Bacteriol 191: 4854-4862.
32. Romero P, Garcia E, Mitchell TJ, (2009) Development of a prophage typing system and analysis of prophage carriage in Streptococcus pneumoniae. Appl Environ Microbiol 75: 1642-1649.
33. Mitchell J, Siboo IR, Takamatsu D, Chambers HF, Sullam PM, (2007) Mechanism of cell surface expression of the Streptococcus mitis platelet binding proteins PblA and PblB. Mol Microbiol 64: 844-857.
34. Bensing BA, Rubens CE, Sullam PM, (2001) Genetic loci of Streptococcus mitis that mediate binding to human platelets. Infect Immun 69: 1373-1380.
35. Mitchell J, Sullam PM, (2009) Streptococcus mitis phage-encoded adhesins mediate attachment to {alpha}2-8-linked sialic acid residues on platelet membrane gangliosides. Infect Immun 77: 3485-3490.
36. Seo HS, Xiong YQ, Mitchell J, Seepersaud R, Bayer AS, et al. (2010) Bacteriophage lysin mediates the binding of Streptococcus mitis to human platelets through interaction with fibrinogen. PLoS Pathog 6.
37. Berry AM, Lock RA, Hansman D, Paton JC, (1989) Contribution of autolysin to virulence of Streptococcus pneumoniae. Infect Immun 57: 2324-2330.
38. Berry AM, Paton JC, (2000) Additive attenuation of virulence of Streptococcus pneumoniae by mutation of the genes encoding pneumolysin and other putative pneumococcal virulence proteins. Infect Immun 68: 133-140.
39. Canvin JR, Marvin AP, Sivakumaran M, Paton JC, Boulnois GJ, et al. (1995) The role of pneumolysin and autolysin in the pathology of pneumonia and septicemia in mice infected with a type 2 pneumococcus. J Infect Dis 172: 119-123.
40. Martner A, Skovbjerg S, Paton JC, Wold AE, (2009) Streptococcus pneumoniae autolysis prevents phagocytosis and production of phagocyte-activating cytokines. Infect Immun 77: 3826-3837.
41. Stroeher UH, Kidd SP, Stafford SL, Jennings MP, Paton JC, et al. (2007) A pneumococcal MerR-like regulator and S-nitrosoglutathione reductase are required for systemic virulence. J Infect Dis 196: 1820-1826.
42. Brown JS, Gilliland SM, Spratt BG, Holden DW, (2004) A locus contained within a variable region of pneumococcal pathogenicity island 1 contributes to virulence in mice. Infect Immun 72: 1587-1593.
43. Croucher NJ, Walker D, Romero P, Lennard N, Paterson GK, et al. (2009) Role of conjugative elements in the evolution of the multidrug-resistant pandemic clone Streptococcus pneumoniae Spain23F ST81. J Bacteriol 191: 1480-1489.
44. Khoo SK, Loll B, Chan WT, Shoeman RL, Ngoo L, et al. (2007) Molecular and structural characterization of the PezAT chromosomal toxin-antitoxin system of the human pathogen Streptococcus pneumoniae. J Biol Chem 282: 19606-19618.
45. Hollands A, Aziz RK, Kansal R, Kotb M, Nizet V, et al. (2008) A naturally occurring mutation in ropB suppresses SpeB expression and reduces M1T1 group A streptococcal systemic virulence. PLoS One 3: e4102.
46. Poulsen K, Reinholdt J, Kilian M, (1996) Characterization of the Streptococcus pneumoniae immunoglobulin A1 protease gene (iga) and its translation product. Infect Immun 64: 3957-3966.
47. Oggioni MR, Memmi G, Maggi T, Chiavolini D, Iannelli F, et al. (2003) Pneumococcal zinc metalloproteinase ZmpC cleaves human matrix metalloproteinase 9 and is a virulence factor in experimental pneumonia. Mol Microbiol 49: 795-805.
48. Chiavolini D, Memmi G, Maggi T, Iannelli F, Pozzi G, et al. (2003) The three extra-cellular zinc metalloproteinases of Streptococcus pneumoniae have a different impact on virulence in mice. BMC Microbiol 3: 14.
49. Kilian M, Mestecky J, Schrohenloher RE, (1979) Pathogenic species of the genus Haemophilus and Streptococcus pneumoniae produce immunoglobulin A1 protease. Infect Immun 26: 143-149.
50. Weiser JN, Bae D, Fasching C, Scamurra RW, Ratner AJ, et al. (2003) Antibody-enhanced pneumococcal adherence requires IgA1 protease. Proc Natl Acad Sci U S A 100: 4215-4220.
51. Kilian M, Reinholdt J, Lomholt H, Poulsen K, Frandsen EV, (1996) Biological significance of IgA1 proteases in bacterial colonization and pathogenesis: critical evaluation of experimental evidence. APMIS 104: 321-338.
52. Wani JH, Gilbert JV, Plaut AG, Weiser JN, (1996) Identification, cloning, and sequencing of the immunoglobulin A1 protease gene of Streptococcus pneumoniae. Infect Immun 64: 3967-3974.
53. Camilli R, Pettini E, Del Grosso M, Pozzi G, Pantosti A, et al. (2006) Zinc metalloproteinase genes in clinical isolates of Streptococcus pneumoniae: association of the full array with a clonal cluster comprising serotypes 8 and 11A. Microbiology 152: 313-321.
54. Henderson-Begg SK, Roberts AP, Hall LM, (2009) Diversity of putative Tn5253-like elements in Streptococcus pneumoniae. Int J Antimicrob Agents 33: 364-367.
55. Ayoubi P, Kilic AO, Vijayakumar MN, (1991) Tn5253, the pneumococcal omega (cat tet) BM6001 element, is a composite structure of two conjugative transposons, Tn5251 and Tn5252. J Bacteriol 173: 1617-1622.
56. Munoz-Najar U, Vijayakumar MN, (1999) An operon that confers UV resistance by evoking the SOS mutagenic response in streptococcal conjugative transposon Tn5252. J Bacteriol 181: 2782-2788.
57. Smith BT, Walker GC, (1998) Mutagenesis and more: umuDC and the Escherichia coli SOS response. Genetics 148: 1599-1610.
58. McAllister LJ, Tseng HJ, Ogunniyi AD, Jennings MP, McEwan AG, et al. (2004) Molecular analysis of the psa permease complex of Streptococcus pneumoniae. Mol Microbiol 53: 889-901.
59. Brown JS, Gilliland SM, Holden DW, (2001) A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence. Mol Microbiol 40: 572-585.
60. Berry AM, Paton JC, (1996) Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect Immun 64: 5255-5262.
61. Brown JS, Gilliland SM, Ruiz-Albert J, Holden DW, (2002) Characterization of pit, a Streptococcus pneumoniae iron uptake ABC transporter. Infect Immun 70: 4389-4398.
62. Dintilhac A, Alloing G, Granadel C, Claverys JP, (1997) Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol Microbiol 25: 727-739.
63. Tseng HJ, McEwan AG, Paton JC, Jennings MP, (2002) Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress. Infect Immun 70: 1635-1639.
64. Busenlehner LS, Pennella MA, Giedroc DP, (2003) The SmtB/ArsR family of metalloregulatory transcriptional repressors: Structural insights into prokaryotic metal resistance. FEMS Microbiol Rev 27: 131-143.
65. Embry A, Hinojosa E, Orihuela CJ, (2007) Regions of Diversity 8, 9 and 13 contribute to Streptococcus pneumoniae virulence. BMC Microbiol 7: 80.
66. Quentin Y, Fichant G, Denizot F, (1999) Inventory, assembly and analysis of Bacillus subtilis ABC transport systems. J Mol Biol 287: 467-484.
67. Hava DL, Camilli A, (2002) Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol 45: 1389-1406.
68. Lau GW, Haataja S, Lonetto M, Kensit SE, Marra A, et al. (2001) A functional genomic analysis of type 3 Streptococcus pneumoniae virulence. Mol Microbiol 40: 555-571.
69. Paterson GK, Nieminen L, Jefferies JM, Mitchell TJ, (2008) PclA, a pneumococcal collagen-like protein with selected strain distribution, contributes to adherence and invasion of host cells. FEMS Microbiol Lett 285: 170-176.
70. 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.
71. Avery OT, Macleod CM, McCarty M, (1944) Studies on the Chemical Nature of the Substance Inducing Transformation of Pneumococcal Types: Induction of Transformation by a Desoxyribonucleic Acid Fraction Isolated from Pneumococcus Type Iii. J Exp Med 79: 137-158.
72. Weiser JN, Austrian R, Sreenivasan PK, Masure HR, (1994) Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. Infect Immun 62: 2582-2589.
73. Horton RM, Ho SN, Pullen JK, Hunt HD, Cai Z, et al. (1993) Gene splicing by overlap extension. Methods Enzymol 217: 270-279.
74. Morona JK, Miller DC, Morona R, Paton JC, (2004) The effect that mutations in the conserved capsular polysaccharide biosynthesis genes cpsA, cpsB, and cpsD have on virulence of Streptococcus pneumoniae. J Infect Dis 189: 1905-1913.
75. LeMessurier KS, Ogunniyi AD, Paton JC, (2006) Differential expression of key pneumococcal virulence genes in vivo. Microbiology 152: 305-311.
76. Ogunniyi AD, Giammarinaro P, Paton JC, (2002) The genes encoding virulence-associated proteins and the capsule of Streptococcus pneumoniae are upregulated and differentially expressed in vivo. Microbiology 148: 2045-2053.
77. Mahdi LK, Ogunniyi AD, LeMessurier KS, Paton JC, (2008) Pneumococcal virulence gene expression and host cytokine profiles during pathogenesis of invasive disease. Infect Immun 76: 646-657.
78. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method. Methods 25: 402-408.
79. Sambrook J, Fritsch EF, Maniatis T, Cold Spring Harbor Laboratory (1989) Molecular cloning: a laboratory manual Cold Spring Harbor Cold Spring Harbor Laboratory Press.
80. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, et al. (2005) ACT: the Artemis Comparison Tool. Bioinformatics 21: 3422-3423.
81. Macrina FL, Evans RP, Tobian JA, Hartley DL, Clewell DB, et al. (1983) Novel shuttle plasmid vehicles for Escherichia-Streptococcus transgeneric cloning. Gene 25: 145-150.
82. Giammarinaro P, Paton JC, (2002) Role of RegM, a homologue of the catabolite repressor protein CcpA, in the virulence of Streptococcus pneumoniae. Infect Immun 70: 5454-5461.
83. Martin B, Garcia P, Castanie MP, Glise B, Claverys JP, (1995) The recA gene of Streptococcus pneumoniae is part of a competence-induced operon and controls an SOS regulon. Dev Biol Stand 85: 293-300.