Role of the single-stranded dna-binding protein ssbb in pneumococcal transformation: Maintenance of a reservoir for genetic plasticity

PLoS Genetics

Volumn 7, Issue 6, 2011, Pages

  Attaiech, Laetitia ^a,b   Olivier, Audrey ^a,b   Mortier Barrière, Isabelle ^a,b   Soulet, Anne Lise ^a,b   Granadel, Chantal ^a,b   Martin, Bernard ^a,b   Polard, Patrice ^a,b   Claverys, Jean Pierre ^a,b  

^a CNRS   (France)

^b UPS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SSBB; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; DNA BINDING PROTEIN; SINGLE STRANDED DNA;

ARTICLE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIUM MUTANT; BACTERIUM TRANSFORMATION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENETIC RECOMBINATION; NONHUMAN; PLASMID; PROTEIN DNA BINDING; PROTEIN INTERACTION; STREPTOCOCCUS PNEUMONIAE; BACTERIAL CHROMOSOME; BIOLOGICAL MODEL; GENETICS; METABOLISM; MUTATION;

BACILLUS SUBTILIS; STREPTOCOCCUS PNEUMONIAE;

BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; DNA, BACTERIAL; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; MODELS, BIOLOGICAL; MUTATION; PLASMIDS; STREPTOCOCCUS PNEUMONIAE; TRANSFORMATION, BACTERIAL;

EID: 79959818880     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002156     Document Type: Article

References (46)

1. Hiller NL, Ahmed A, Powell E, Martin DP, Eutsey R, 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 doi:10.1371/journal.ppat.1001108.
2. 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.
3. Lacks S, Greenberg B, Carlson K, (1967) Fate of donor DNA in pneumococcal transformation. J Mol Biol 29: 327-347.
4. Dagkessamanskaia A, Moscoso M, Hénard V, Guiral S, Overweg K, et al. (2004) Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells. Mol Microbiol 51: 1071-1086.
5. Peterson S, Sung CK, Cline R, Desai BV, Snesrud E, et al. (2004) Identification of competence pheromone responsive genes in Streptococcus pneumoniae. Mol Microbiol 51: 1051-1070.
6. Håvarstein LS, Coomaraswamy G, Morrison DA, (1995) An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc Natl Acad Sci USA 92: 11140-11144.
7. Claverys JP, Håvarstein LS, (2002) Extra-cellular peptide control of competence for genetic transformation in Streptococcus pneumoniae. Frontiers in Biosci 7: 1798-1814.
8. Claverys JP, Prudhomme M, Martin B, (2006) Induction of competence regulons as general stress responses in Gram-positive bacteria. Annu Rev Microbiol 60: 451-475.
9. Ephrussi-Taylor H, (1960) L'état du DNA transformant au cours des premières phases de la transformation bactérienne. C R Soc Biol 154: 1951-1955.
10. Miao R, Guild WR, (1970) Competent Diplococcus pneumoniae accept both single- and double-stranded deoxyribonucleic acid. J Bacteriol 101: 361-364.
11. Morrison DA, Mannarelli B, (1979) Transformation in pneumococcus: nuclease resistance of deoxyribonucleic acid in eclipse complex. J Bacteriol 140: 655-665.
12. Morrison DA, (1977) Transformation in pneumococcus: existence and properties of a complex involving donor deoxyribonucleate single strands in eclipse. J Bacteriol 132: 576-583.
13. Morrison DA, Baker M, (1979) Competence for genetic transformation in pneumococcus depends on synthesis of a small set of proteins. Nature 282: 215-217.
14. Morrison DA, Baker M, Mannarelli B, (1979) Transformation- 1978 pp. 43-52 Cotswold Press Ltd, Oxford, U.K.
15. Morrison DA, Mortier-Barrière I, Attaiech L, Claverys JP, (2007) Identification of the Major Protein Component of the Pneumococcal Eclipse Complex. J Bacteriol 189: 6497-6500.
16. Claverys JP, Martin B, Polard P, (2009) The genetic transformation machinery: composition, localization and mechanism. FEMS Microbiol Rev 33: 643-656.
17. Thanassi JA, Hartman-Neumann SL, Dougherty TJ, Dougherty BA, Pucci MJ, (2002) Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae. Nucleic Acids Res 30: 3152-3162.
18. Campbell EA, Choi SY, Masure HR, (1998) A competence regulon in Streptococcus pneumoniae revealed by genomic analysis. Mol Microbiol 27: 929-939.
19. Bergé M, Mortier-Barrière I, Martin B, Claverys JP, (2003) Transformation of Streptococcus pneumoniae relies on DprA- and RecA-dependent protection of incoming single strands. Mol Microbiol 50: 527-536.
20. Mortier-Barrière I, Velten M, Dupaigne P, Mirouze N, Piétrement O, et al. (2007) A key presynaptic role in transformation for a widespread bacterial protein: DprA conveys incoming ssDNA to RecA. Cell 130: 824-836.
21. Berka RM, Hahn J, Albano M, Draskovic I, Persuh M, et al. (2002) Microarray analysis of the Bacillus subtilis K-state: genome-wide expression changes dependent on ComK. Mol Microbiol 43: 1331-1345.
22. Ogura M, Yamaguchi H, Kobayashi K, Ogasawara N, Fujita Y, et al. (2002) Whole-genome analysis of genes regulated by the Bacillus subtilis competence transcription factor ComK. J Bacteriol 184: 2344-2351.
23. Lindner C, Nijland R, van Hartskamp M, Bron S, Hamoen L, et al. (2004) Differential expression of two paralogous genes of Bacillus subtilis encoding single-stranded DNA binding protein. J Bacteriol 186: 1097-1105.
24. Grove DE, Bryant FR, (2006) Effect of Mg2+ on the DNA binding modes of the Streptococcus pneumoniae SsbA and SsbB proteins. J Biol Chem 281: 2087-2094.
25. Shereda RD, Kozlov AG, Lohman TM, Cox MM, Keck JL, (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit Rev Biochem Mol Biol 43: 289-318.
26. Costes A, Lecointe F, McGovern S, Quevillon-Cheruel S, Polard P, (2010) The C-Terminal Domain of the Bacterial SSB Protein Acts as a DNA Maintenance Hub at Active Chromosome Replication Forks. PLoS Genet 6: e1001238 doi:10.1371/journal.pgen.1001238.
27. Méjean V, Claverys JP, (1984) Use of a cloned fragment to analyze the fate of donor DNA in transformation of Streptococcus pneumoniae. J Bacteriol 158: 1175-1178.
28. Saunders CW, Guild WR, (1981) Pathway of plasmid transformation in pneumococcus: open circular and linear molecules are active. J Bacteriol 146: 517-526.
29. Morrison DA, Guild WR, (1973) Breakage prior to entry of DNA in Pneumococcus transformation. Biochim Biophys Acta 299: 545-556.
30. Claverys JP, Håvarstein LS, (2007) Cannibalism and fratricide: mechanisms and raisons d'être. Nat Rev Microbiol 5: 219-229.
31. Claverys JP, Martin B, Håvarstein LS, (2007) Competence-induced fratricide in streptococci. Mol Microbiol 64: 1423-1433.
32. Bernstein H, Byerly HC, Hopf FA, Michod RE, (1985) The evolutionary role of recombinational repair and sex. Int Rev Cytol 96: 1-24.
33. Dubnau D, (1999) DNA uptake in bacteria. Annu Rev Microbiol 53: 217-244.
34. Grove DE, Willcox S, Griffith JD, Bryant FR, (2005) Differential single-stranded DNA binding properties of the paralogous SsbA and SsbB proteins from Streptococcus pneumoniae. J Biol Chem 280: 11067-11073.
35. Saunders CW, Guild WR, (1981) Monomer plasmid DNA transforms Streptococcus pneumoniae. Mol Gen Genet 181: 57-62.
36. Kantake N, Madiraju MV, Sugiyama T, Kowalczykowski SC, (2002) Escherichia coli RecO protein anneals ssDNA complexed with its cognate ssDNA-binding protein: A common step in genetic recombination. Proc Natl Acad Sci USA 99: 15327-15332.
37. Kidane D, Carrasco B, Manfredi C, Rothmaier K, Ayora S, et al. (2009) Evidence for different pathways during horizontal gene transfer in competent Bacillus subtilis cells. PLoS Genet 5: e1000630 doi:10.1371/journal.pgen.1000630.
38. Sibold C, Markiewicz Z, Latorre C, Hakenbeck R, (1991) Novel plasmids in clinical strains of Streptococcus pneumoniae. FEMS Microbiol Lett 77: 91-96.
39. Pozzi G, Masala L, Iannelli F, Manganelli R, Håvarstein LS, et al. (1996) Competence for genetic transformation in Streptococcus pneumoniae: two allelic variants of the peptide pheromone. J Bacteriol 178: 6087-6090.
40. Saunders CW, Guild WR, (1980) Properties and transforming activities of two plasmids in Streptococcus pneumoniae. Mol Gen Genet 180: 573-578.
41. Séréna C, (2005) Etude moléculaire de la protéine SSB de Bacillus subtilis. Ph D Dissertation, Université Paris XI, Orsay, France.
42. Prudhomme M, Camilli A, Claverys JP, (2007) The Molecular Biology of Streptococci pp. 511-518 Horizon Scientific Press, Norfolk, UK.
43. Cartee RT, Forsee WT, Bender MH, Ambrose KD, Yother J, (2005) CpsE from type 2 Streptococcus pneumoniae catalyzes the reversible addition of glucose-1-phosphate to a polyprenyl phosphate acceptor, initiating type 2 capsule repeat unit formation. J Bacteriol 187: 7425-7433.
44. Lanie JA, Ng WL, Kazmierczak KM, Andrzejewski TM, Davidsen TM, et al. (2007) Genome Sequence of Avery's Virulent Serotype 2 Strain D39 of Streptococcus pneumoniae and Comparison with That of Unencapsulated Laboratory Strain R6. J Bacteriol 189: 38-51.
45. Martin B, Prudhomme M, Alloing G, Granadel C, Claverys JP, (2000) Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Mol Microbiol 38: 867-878.
46. Bergé M, Moscoso M, Prudhomme M, Martin B, Claverys JP, (2002) Uptake of transforming DNA in Gram-positive bacteria: a view from Streptococcus pneumoniae. Mol Microbiol 45: 411-421.