Home LiteratureArticle Details
PMID: 17041037 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6.

Journal of bacteriology ·Vol. 189 ·No. 1 ·2007-01-00 ·Pages 38-51

Lanie JA, Ng WL, Kazmierczak KM, Andrzejewski TM, Davidsen TM, Wayne KJ, Tettelin H, Glass JI, Winkler ME

Abstract

Streptococcus pneumoniae (pneumococcus) is a leading human respiratory pathogen that causes a variety of serious mucosal and invasive diseases. D39 is an historically important serotype 2 strain that was used in experiments by Avery and coworkers to demonstrate that DNA is the genetic material. Although isolated nearly a century ago, D39 remains extremely virulent in murine infection models and is perhaps the strain used most frequently in current studies of pneumococcal pathogenesis. To date, the complete genome sequences have been reported for only two S. pneumoniae strains: TIGR4, a recent serotype 4 clinical isolate, and laboratory strain R6, an avirulent, unencapsulated derivative of strain D39. We report here the genome sequences and new annotation of two different isolates of strain D39 and the corrected sequence of strain R6. Comparisons of these three related sequences allowed deduction of the likely sequence of the D39 progenitor and mutations that arose in each isolate. Despite its numerous repeated sequences and IS elements, the serotype 2 genome has remained remarkably stable during cultivation, and one of the D39 isolates contains only five relatively minor mutations compared to the deduced D39 progenitor. In contrast, laboratory strain R6 contains 71 single-base-pair changes, six deletions, and four insertions and has lost the cryptic pDP1 plasmid compared to the D39 progenitor strain. Many of these mutations are in or affect the expression of genes that play important roles in regulation, metabolism, and virulence. The nature of the mutations that arose spontaneously in these three strains, the relative global transcription patterns determined by microarray analyses, and the implications of the D39 genome sequences to studies of pneumococcal physiology and pathogenesis are presented and discussed.

MeSH Terms
Animals DNA Transposable Elements/genetics Genome, Bacterial Humans Male Mice Mice, Inbred ICR Microarray Analysis Molecular Sequence Data Mutation Pneumococcal Infections/microbiology Sequence Homology, Nucleic Acid Streptococcus pneumoniae/genetics,pathogenicity Virulence
Chemicals
DNA Transposable Elements
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Lanie Joel A
Department of Biology, Indiana University Bloomington, Jordan Hall 142, Bloomington, IN 47405, USA.
Ng Wai-Leung
Kazmierczak Krystyna M
Andrzejewski Tiffany M
Davidsen Tanja M
Wayne Kyle J
Tettelin Hervé
Glass John I
Winkler Malcolm E
References (104)
104 references, click to expand
  1. Molecular basis of the optochin-sensitive phenotype of pneumococcus: characterization of the genes encoding the F0 complex of the Streptococcus pneumoniae and Streptococcus oralis H(+)-ATPases.
    Mol Microbiol. 1994 May;12(4):587-98 PMID: 7934882
  2. Cloning and characterization of the gene encoding a novel beta-galactosidase from Bacillus circulans.
    Biosci Biotechnol Biochem. 1997 Aug;61(8):1270-6 PMID: 9301106
  3. Genomic diversity between strains of the same serotype and multilocus sequence type among pneumococcal clinical isolates.
    Infect Immun. 2006 Jun;74(6):3513-8 PMID: 16714583
  4. Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the fenton reaction.
    J Bacteriol. 2003 Dec;185(23):6815-25 PMID: 14617646
  5. The genetic basis of colony opacity in Streptococcus pneumoniae: evidence for the effect of box elements on the frequency of phenotypic variation.
    Mol Microbiol. 1995 Apr;16(2):215-27 PMID: 7565084
  6. Current trends in capsular polysaccharide biosynthesis of Streptococcus pneumoniae.
    Res Microbiol. 2000 Jul-Aug;151(6):429-35 PMID: 10961455
  7. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
    J Mol Biol. 2001 Jan 19;305(3):567-80 PMID: 11152613
  8. A plasmid in Streptococcus pneumoniae.
    J Bacteriol. 1979 Feb;137(2):735-9 PMID: 33961
  9. The PROSITE database, its status in 2002.
    Nucleic Acids Res. 2002 Jan 1;30(1):235-8 PMID: 11752303
  10. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae.
    Science. 2001 Jul 20;293(5529):498-506 PMID: 11463916
  11. Constitutive expression of PcsB suppresses the requirement for the essential VicR (YycF) response regulator in Streptococcus pneumoniae R6.
    Mol Microbiol. 2003 Dec;50(5):1647-63 PMID: 14651645
  12. An rpsL cassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae.
    Appl Environ Microbiol. 2001 Nov;67(11):5190-6 PMID: 11679344
  13. Characterization of cryptic plasmids pDP1 and pSMB1 of Streptococcus pneumoniae.
    Plasmid. 1999 Jan;41(1):70-2 PMID: 9887308
  14. Streptolydigin resistance can be conferred by alterations to either the beta or beta' subunits of Bacillus subtilis RNA polymerase.
    J Biol Chem. 1995 Oct 13;270(41):23930-3 PMID: 7592585
  15. New insights into the pneumococcal fratricide: relationship to clumping and identification of a novel immunity factor.
    Mol Microbiol. 2006 Feb;59(4):1297-307 PMID: 16430701
  16. Sequence analysis and characterization of a novel fibronectin-binding repeat domain from the surface of Streptococcus pneumoniae.
    OMICS. 2004 Winter;8(4):341-56 PMID: 15703481
  17. Requirement for capsule in colonization by Streptococcus pneumoniae.
    Infect Immun. 2001 Jun;69(6):3755-61 PMID: 11349040
  18. Microbial gene identification using interpolated Markov models.
    Nucleic Acids Res. 1998 Jan 15;26(2):544-8 PMID: 9421513
  19. Pyruvate oxidase is a determinant of Avery's rough morphology.
    J Bacteriol. 2004 Dec;186(24):8164-71 PMID: 15576764
  20. Diversity and evolution of protein translocation.
    Annu Rev Microbiol. 2005;59:91-111 PMID: 16153164
  21. An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11140-4 PMID: 7479953
  22. Short-sequence tandem and nontandem DNA repeats and endogenous hydrogen peroxide production contribute to genetic instability of Streptococcus pneumoniae.
    J Bacteriol. 2002 Aug;184(16):4392-9 PMID: 12142409
  23. 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. 1944 Feb 1;79(2):137-58 PMID: 19871359
  24. Role of RegM, a homologue of the catabolite repressor protein CcpA, in the virulence of Streptococcus pneumoniae.
    Infect Immun. 2002 Oct;70(10):5454-61 PMID: 12228270
  25. Mosaic genes and mosaic chromosomes: intra- and interspecies genomic variation of Streptococcus pneumoniae.
    Infect Immun. 2001 Apr;69(4):2477-86 PMID: 11254610
  26. Penicillin tolerance in Streptococcus pneumoniae, autolysis and the Psa ATP-binding cassette (ABC) manganese permease.
    Mol Microbiol. 1999 May;32(4):881-3 PMID: 10361289
  27. Pneumococcal disease and the role of conjugate vaccines.
    Microb Drug Resist. 1999 Summer;5(2):147-57 PMID: 10432276
  28. Encoded errors: mutations and rearrangements mediated by misalignment at repetitive DNA sequences.
    Mol Microbiol. 2004 Jun;52(5):1243-53 PMID: 15165229
  29. Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements.
    Proc Natl Acad Sci U S A. 2005 Jun 14;102(24):8710-5 PMID: 15928084
  30. The structural biology of type II fatty acid biosynthesis.
    Annu Rev Biochem. 2005;74:791-831 PMID: 15952903
  31. Strategies for the control of pneumococcal diseases.
    Vaccine. 1999 Jul 30;17 Suppl 1:S79-84 PMID: 10471187
  32. Frequent oligonucleotide motifs in genomes of three streptococci.
    Nucleic Acids Res. 2002 Oct 1;30(19):4216-21 PMID: 12364600
  33. A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli.
    J Bacteriol. 2004 Feb;186(3):785-93 PMID: 14729705
  34. Molecular characterization of PcpA: a novel choline-binding protein of Streptococcus pneumoniae.
    FEMS Microbiol Lett. 1998 Jul 1;164(1):207-14 PMID: 9675866
  35. The COG database: an updated version includes eukaryotes.
    BMC Bioinformatics. 2003 Sep 11;4:41 PMID: 12969510
  36. Identification of two genes, cpsX and cpsY, with putative regulatory function on capsule expression in group B streptococci.
    FEMS Immunol Med Microbiol. 1998 Jun;21(2):159-68 PMID: 9685006
  37. Organ-specific models of Streptococcus pneumoniae disease.
    Scand J Infect Dis. 2003;35(9):647-52 PMID: 14620149
  38. 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. 1997 Aug;25(4):727-39 PMID: 9379902
  39. Solution structure and function of an essential CMP kinase of Streptococcus pneumoniae.
    Protein Sci. 2003 Nov;12(11):2613-21 PMID: 14573872
  40. The pavA gene of Streptococcus pneumoniae encodes a fibronectin-binding protein that is essential for virulence.
    Mol Microbiol. 2001 Sep;41(6):1395-408 PMID: 11580843
  41. Differential fluorescence induction analysis of Streptococcus pneumoniae identifies genes involved in pathogenesis.
    Infect Immun. 2002 Mar;70(3):1422-33 PMID: 11854229
  42. ZmpB, a novel virulence factor of Streptococcus pneumoniae that induces tumor necrosis factor alpha production in the respiratory tract.
    Infect Immun. 2003 Sep;71(9):4925-35 PMID: 12933834
  43. From nose to lung: the regulation behind Streptococcus pneumoniae virulence factors.
    Mol Microbiol. 2003 Nov;50(4):1103-10 PMID: 14622402
  44. Improved prediction of signal peptides: SignalP 3.0.
    J Mol Biol. 2004 Jul 16;340(4):783-95 PMID: 15223320
  45. Gene disruption studies of penicillin-binding proteins 1a, 1b, and 2a in Streptococcus pneumoniae.
    J Bacteriol. 1999 Oct;181(20):6552-5 PMID: 10515951
  46. The Ami-AliA/AliB permease of Streptococcus pneumoniae is involved in nasopharyngeal colonization but not in invasive disease.
    Infect Immun. 2004 Jul;72(7):3902-6 PMID: 15213133
  47. Contribution of a response regulator to the virulence of Streptococcus pneumoniae is strain dependent.
    Infect Immun. 2003 Aug;71(8):4405-13 PMID: 12874319
  48. Streptococcus pneumoniae: virulence factors, pathogenesis, and vaccines.
    Microbiol Rev. 1995 Dec;59(4):591-603 PMID: 8531887
  49. Tissue-specific contributions of pneumococcal virulence factors to pathogenesis.
    J Infect Dis. 2004 Nov 1;190(9):1661-9 PMID: 15478073
  50. The Listeria monocytogenes gene ctpA encodes a putative P-type ATPase involved in copper transport.
    Mol Gen Genet. 1997 Jan 27;253(4):484-91 PMID: 9037109
  51. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence.
    Nucleic Acids Res. 1997 Mar 1;25(5):955-64 PMID: 9023104
  52. Novel plasmids in clinical strains of Streptococcus pneumoniae.
    FEMS Microbiol Lett. 1991 Jan 1;61(1):91-5 PMID: 2004700
  53. MurA (MurZ), the enzyme that catalyzes the first committed step in peptidoglycan biosynthesis, is essential in Escherichia coli.
    J Bacteriol. 1995 Jul;177(14):4194-7 PMID: 7608103
  54. Regulation of Streptococcus pneumoniae clp genes and their role in competence development and stress survival.
    J Bacteriol. 2001 Dec;183(24):7295-307 PMID: 11717289
  55. Growth and division of Streptococcus pneumoniae: localization of the high molecular weight penicillin-binding proteins during the cell cycle.
    Mol Microbiol. 2003 Nov;50(3):845-55 PMID: 14617146
  56. Pyruvate oxidase, as a determinant of virulence in Streptococcus pneumoniae.
    Mol Microbiol. 1996 Feb;19(4):803-13 PMID: 8820650
  57. Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes.
    Microbiology. 2005 Dec;151(Pt 12):3895-909 PMID: 16339935
  58. Bacterial transcription elongation factors: new insights into molecular mechanism of action.
    Mol Microbiol. 2005 Mar;55(5):1315-24 PMID: 15720542
  59. A genomic analysis of two-component signal transduction in Streptococcus pneumoniae.
    Mol Microbiol. 2000 Feb;35(3):566-76 PMID: 10672179
  60. Molecular and cellular biology of pneumococcal infection.
    Microb Drug Resist. 1997 Winter;3(4):297-308 PMID: 9442482
  61. Development of competence in Streptococcus pneumonaie: pheromone autoinduction and control of quorum sensing by the oligopeptide permease.
    Mol Microbiol. 1998 Jul;29(1):75-83 PMID: 9701804
  62. PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation.
    Infect Immun. 2005 May;73(5):2680-9 PMID: 15845469
  63. Molecular analysis of the psa permease complex of Streptococcus pneumoniae.
    Mol Microbiol. 2004 Aug;53(3):889-901 PMID: 15255900
  64. The simple sequence contingency loci of Haemophilus influenzae and Neisseria meningitidis.
    J Clin Invest. 2001 Mar;107(6):657-62 PMID: 11254662
  65. Two different dihydroorotate dehydrogenases in Lactococcus lactis.
    J Bacteriol. 1994 Jul;176(13):3975-82 PMID: 8021180
  66. Penicillin tolerance genes of Streptococcus pneumoniae: the ABC-type manganese permease complex Psa.
    Mol Microbiol. 1998 Sep;29(5):1285-96 PMID: 9767595
  67. Improved statistical inference from DNA microarray data using analysis of variance and a Bayesian statistical framework. Analysis of global gene expression in Escherichia coli K12.
    J Biol Chem. 2001 Jun 8;276(23):19937-44 PMID: 11259426
  68. Improved microbial gene identification with GLIMMER.
    Nucleic Acids Res. 1999 Dec 1;27(23):4636-41 PMID: 10556321
  69. Profile hidden Markov models.
    Bioinformatics. 1998;14(9):755-63 PMID: 9918945
  70. A functional genomic analysis of type 3 Streptococcus pneumoniae virulence.
    Mol Microbiol. 2001 May;40(3):555-71 PMID: 11359563
  71. The ami locus of the gram-positive bacterium Streptococcus pneumoniae is similar to binding protein-dependent transport operons of gram-negative bacteria.
    Mol Microbiol. 1990 Apr;4(4):633-44 PMID: 2352474
  72. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  73. Regulation of growth inhibition at high temperature, autolysis, transformation and adherence in Streptococcus pneumoniae by clpC.
    Mol Microbiol. 2000 Aug;37(4):717-26 PMID: 10972795
  74. The type 2 capsule locus of Streptococcus pneumoniae.
    J Bacteriol. 1999 Apr;181(8):2652-4 PMID: 10198036
  75. The carB gene encoding the large subunit of carbamoylphosphate synthetase from Lactococcus lactis is transcribed monocistronically.
    J Bacteriol. 1998 Sep;180(17):4380-6 PMID: 9721272
  76. Purification and polar localization of pneumococcal LytB, a putative endo-beta-N-acetylglucosaminidase: the chain-dispersing murein hydrolase.
    J Bacteriol. 2002 Sep;184(18):4988-5000 PMID: 12193614
  77. Mosaic genes and mosaic chromosomes-genomic variation in Streptococcus pneumoniae.
    Int J Med Microbiol. 2004 Sep;294(2-3):157-68 PMID: 15493826
  78. Choline-binding protein D (CbpD) in Streptococcus pneumoniae is essential for competence-induced cell lysis.
    J Bacteriol. 2005 Jul;187(13):4338-45 PMID: 15968042
  79. Appearance of genetic transforming activity in pneumococcal cultures.
    Science. 1960 Oct 28;132(3435):1257-8 PMID: 13731684
  80. Annotated draft genomic sequence from a Streptococcus pneumoniae type 19F clinical isolate.
    Microb Drug Resist. 2001 Summer;7(2):99-125 PMID: 11442348
  81. MUSCLE: multiple sequence alignment with high accuracy and high throughput.
    Nucleic Acids Res. 2004;32(5):1792-7 PMID: 15034147
  82. Differential expression of key pneumococcal virulence genes in vivo.
    Microbiology. 2006 Feb;152(Pt 2):305-11 PMID: 16436418
  83. Visualizing pneumococcal infections in the lungs of live mice using bioluminescent Streptococcus pneumoniae transformed with a novel gram-positive lux transposon.
    Infect Immun. 2001 May;69(5):3350-8 PMID: 11292758
  84. Genome of the bacterium Streptococcus pneumoniae strain R6.
    J Bacteriol. 2001 Oct;183(19):5709-17 PMID: 11544234
  85. In vivo characterization of the psa genes from Streptococcus pneumoniae in multiple models of infection.
    Microbiology. 2002 May;148(Pt 5):1483-91 PMID: 11988523
  86. Invasive pneumococcal disease in the immunocompromised host.
    Microb Drug Resist. 1997 Fall;3(3):215-32 PMID: 9270991
  87. Catabolite control protein A (CcpA) contributes to virulence and regulation of sugar metabolism in Streptococcus pneumoniae.
    J Bacteriol. 2005 Dec;187(24):8340-9 PMID: 16321938
  88. Domain organization and molecular characterization of 13 two-component systems identified by genome sequencing of Streptococcus pneumoniae.
    Gene. 1999 Sep 3;237(1):223-34 PMID: 10524254
  89. The Streptococcus pneumoniae cia regulon: CiaR target sites and transcription profile analysis.
    J Bacteriol. 2003 Jan;185(1):60-70 PMID: 12486041
  90. Role of novel choline binding proteins in virulence of Streptococcus pneumoniae.
    Infect Immun. 2000 Oct;68(10):5690-5 PMID: 10992472
  91. Inactivation of the srtA gene affects localization of surface proteins and decreases adhesion of Streptococcus pneumoniae to human pharyngeal cells in vitro.
    Infect Immun. 2003 May;71(5):2758-65 PMID: 12704150
  92. TIGRFAMs: a protein family resource for the functional identification of proteins.
    Nucleic Acids Res. 2001 Jan 1;29(1):41-3 PMID: 11125044
  93. The Pfam protein families database.
    Nucleic Acids Res. 2000 Jan 1;28(1):263-6 PMID: 10592242
  94. Global transcriptional analysis of clpP mutations of type 2 Streptococcus pneumoniae and their effects on physiology and virulence.
    J Bacteriol. 2002 Jul;184(13):3508-20 PMID: 12057945
  95. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.
    Nat Genet. 2000 May;25(1):25-9 PMID: 10802651
  96. Essentiality of clpX, but not clpP, clpL, clpC, or clpE, in Streptococcus pneumoniae R6.
    J Bacteriol. 2003 May;185(9):2961-6 PMID: 12700276
  97. Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors.
    Mol Microbiol. 2002 Sep;45(5):1389-406 PMID: 12207705
  98. Mutational analysis of the Streptococcus pneumoniae bimodular class A penicillin-binding proteins.
    J Bacteriol. 1999 Jun;181(12):3852-6 PMID: 10368166
  99. A pneumolysin-negative mutant of Streptococcus pneumoniae causes chronic bacteremia rather than acute sepsis in mice.
    Infect Immun. 1995 Feb;63(2):448-55 PMID: 7822009
  100. Contribution of the ATP-dependent protease ClpCP to the autolysis and virulence of Streptococcus pneumoniae.
    Infect Immun. 2005 Feb;73(2):730-40 PMID: 15664911
  101. Resistance among Streptococcus pneumoniae: Implications for drug selection.
    Clin Infect Dis. 2002 Jun 15;34(12):1613-20 PMID: 12032897
  102. Cloning and sequencing of Escherichia coli murZ and purification of its product, a UDP-N-acetylglucosamine enolpyruvyl transferase.
    J Bacteriol. 1992 Sep;174(17):5748-52 PMID: 1512209
  103. Transcription attenuation: a highly conserved regulatory strategy used by bacteria.
    Trends Genet. 2005 May;21(5):260-4 PMID: 15851059
  104. Presence of a small plasmid in clinical isolates of Streptococcus pneumoniae.
    FEMS Microbiol Lett. 1989 Dec;53(3):275-8 PMID: 2693203
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2007-01-00
Epub
2006-00-13
Pages
38-51
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC1797212
Subset
IM
Grants
NIAID NIH HHS · R01 AI060744 · United States
NIAID NIH HHS · AI060744-01 · United States
Databases
GENBANK
CP000410
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]