Structure-function relationships of two paralogous single-stranded DNA-binding proteins from Streptomyces coelicolor: Implication of SsbB in chromosome segregation during sporulation

Nucleic Acids Research

Volumn 41, Issue 6, 2013, Pages 3659-3672

  Paradzik, Tina ^a   Ivic, Nives ^a   Filic, Zelimira ^a   Manjasetty, Babu A ^b   Herron, Paul ^c   Luic, Marija ^a   Vujaklija, Dusica ^a  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^c UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; MESSENGER RNA; SINGLE STRANDED DNA BINDING PROTEIN; TRYPTOPHAN;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIUM MUTANT; BINDING AFFINITY; CELL FUNCTION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; FLUORESCENCE ANALYSIS; FLUORESCENCE MICROSCOPY; FLUORESCENT QUENCHING; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC TRANSCRIPTION; MUTATIONAL ANALYSIS; NONHUMAN; PARALOGY; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN STRUCTURE; RPSF GENE; SPOROGENESIS; SSBA GENE; SSBB GENE; START CODON; STREPTOMYCES COELICOLOR; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION INITIATION SITE;

ACTINOBACTERIA; BACTERIAL PROTEINS; BASE SEQUENCE; CHROMOSOME SEGREGATION; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SPORES, BACTERIAL; STREPTOMYCES COELICOLOR; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION INITIATION SITE;

ACTINOBACTERIA; STREPTOMYCES COELICOLOR;

EID: 84876013386     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt050     Document Type: Article

References (68)

1. Hopwood, D.A. (1999) Forty years of genetics with Streptomyces: from in vivo through in vitro to in silico. Microbiology, 145(Pt 9), 2183-2202.
2. Bentley, S.D., Chater, K.F., Cerdeno-Tarraga, A.M., Challis, G.L., Thomson, N.R., James, K.D., Harris, D.E., Quail, M.A., Kieser, H., Harper, D. et al. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature, 417, 141-147.
3. Szczepankowska, A.K., Prestel, E., Mariadassou, M., Bardowski, J.K. and Bidnenko, E. (2011) Phylogenetic and complementation analysis of a single-stranded DNA binding protein family from lactococcal phages indicates a non-bacterial origin. PLoS One, 6, e26942.
4. Meyer, R.R. and Laine, P.S. (1990) The single-stranded DNA-binding protein of Escherichia coli. Microbiol. Rev., 54, 342-380.
5. Glassberg, J., Meyer, R.R. and Kornberg, A. (1979) Mutant single-strand binding protein of Escherichia coli: genetic and physiological characterization. J. Bacteriol., 140, 14-19.
6. Shereda, R.D., Kozlov, A.G., Lohman, T.M., Cox, M.M. and Keck, J.L. (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit. Rev. Biochem. Mol. Biol., 43, 289-318.
7. Costes, A., Lecointe, F., McGovern, S., Quevillon-Cheruel,S. and 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.
8. Murzin, A.G. (1993) OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. EMBO J., 12, 861-867.
9. Curth, U., Genschel, J., Urbanke,C. and Greipel, J. (1996) In vitro and in vivo function of the C-terminus of Escherichia coli single-stranded DNA binding protein. Nucleic Acids Res., 24, 2706-2711.
10. Raghunathan, S., Ricard, C.S., Lohman, T.M. and Waksman, G. (1997) Crystal structure of the homo-tetrameric DNA binding domain of Escherichia coli single-stranded DNA-binding protein determined by multiwavelength x-ray diffraction on the selenomethionyl protein at 2.9-A resolution. Proc. Natl Acad. Sci. USA, 94, 6652-6657.
11. Stefanic, Z., Vujaklija,D. and Luic, M. (2009) Structure of the single-stranded DNA-binding protein from Streptomyces coelicolor. Acta. Crystallogr. D Biol. Crystallogr., 65, 974-979.
12. Roy, R., Kozlov, A.G., Lohman, T.M. and Ha, T. (2007) Dynamic structural rearrangements between DNA binding modes of E. coli SSB protein. J. Mol. Biol., 369, 1244-1257.
13. Lindner, C., Nijland, R., van Hartskamp, M., Bron, S., Hamoen, L.W. and Kuipers, O.P. (2004) Differential expression of two paralogous genes of Bacillus subtilis encoding single-stranded DNA binding protein. J. Bacteriol., 186, 1097-1105.
14. Yadav, T., Carrasco, B., Myers, A.R., George, N.P., Keck, J.L. and Alonso, J.C. (2012) Genetic recombination in Bacillus subtilis: a division of labor between two single-strand DNA-binding proteins. Nucleic Acids Res., 40, 5546-5559.
15. Grove, D.E., Willcox, S., Griffith, J.D. and Bryant, F.R. (2005) Differential single-stranded DNA binding properties of the paralogous SsbA and SsbB proteins from Streptococcus pneumoniae. J. Biol. Chem., 280, 11067-11073.
16. Flardh, K., Richards, D.M., Hempel, A.M., Howard,M. and Buttner, M.J. (2012) Regulation of apical growth and hyphal branching in Streptomyces. Curr. Opin. Microbiol., 15, 737-743.
17. Ruban-Osmialowska, B., Jakimowicz, D., Smulczyk-Krawczyszyn, A., Chater, K.F. and Zakrzewska-Czerwinska, J. (2006) Replisome localization in vegetative and aerial hyphae of Streptomyces coelicolor. J. Bacteriol., 188, 7311-7316.
18. Flardh,K. and Buttner, M.J. (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat. Rev. Microbiol., 7, 36-49.
19. Jakimowicz,D. and van Wezel, G.P. (2012) Cell division and DNA segregation in Streptomyces: how to build a septum in the middle of nowhere? Mol. Microbiol., 85, 393-404.
20. Wang, L., Yu, Y., He, X., Zhou, X., Deng, Z., Chater, K.F. and Tao, M. (2007) Role of an FtsK-like protein in genetic stability in Streptomyces coelicolor A3(2). J. Bacteriol., 189, 2310-2318.
21. Dedrick, R.M., Wildschutte,H. and McCormick, J.R. (2009) Genetic interactions of smc, ftsK, and parB genes in Streptomyces coelicolor and their developmental genome segregation phenotypes. J. Bacteriol., 191, 320-332.
22. Kois, A., Swiatek, M., Jakimowicz,D. and Zakrzewska-Czerwinska, J. (2009) SMC protein-dependent chromosome condensation during aerial hyphal development in Streptomyces. J. Bacteriol., 191, 310-319.
23. Kim, H.J., Calcutt, M.J., Schmidt, F.J. and Chater, K.F. (2000) Partitioning of the linear chromosome during sporulation of Streptomyces coelicolor A3(2) involves an oriC-linked parAB locus. J. Bacteriol., 182, 1313-1320.
24. Jakimowicz, D., Zydek, P., Kois, A., Zakrzewska-Czerwinska,J. and Chater, K.F. (2007) Alignment of multiple chromosomes along helical ParA scaffolding in sporulating Streptomyces hyphae. Mol. Microbiol., 65, 625-641.
25. Ditkowski, B., Troc, P., Ginda, K., Donczew, M., Chater, K.F., Zakrzewska-Czerwinska,J. and Jakimowicz, D. (2010) The actinobacterial signature protein ParJ (SCO1662) regulates ParA polymerization and affects chromosome segregation and cell division during Streptomyces sporulation. Mol. Microbiol., 78, 1403-1415.
26. Pigac,J. and Schrempf, H. (1995) A simple and rapid method of transformation of Streptomyces rimosus r6 and other streptomycetes by electroporation. Appl. Environ. Microbiol., 61, 352-356.
27. Kieser, T.B., Buttner, M.J., Chater, K.F. and Hopwood, D.A. (2000) Practical Streptomyces Genetics. The John Innes Foundation, Norwich.
28. Mijakovic, I., Petranovic, D., Macek, B., Cepo, T., Mann, M., Davies, J., Jensen, P.R. and Vujaklija, D. (2006) Bacterial single-stranded DNA-binding proteins are phosphorylated on tyrosine. Nucleic Acids Res., 34, 1588-1596.
29. Waters, B., Vujaklija, D., Gold, M.R. and Davies, J. (1994) Protein tyrosine phosphorylation in streptomycetes. FEMS Microbiol. Lett., 120, 187-190.
30. Fernandez-Martinez, L.T., Del Sol, R., Evans, M.C., Fielding, S., Herron, P.R., Chandra,G. and Dyson, P.J. (2011) A transposon insertion single-gene knockout library and new ordered cosmid library for the model organism Streptomyces coelicolor A3(2). Antonie Van Leeuwenhoek, 99, 515-522.
31. Gust, B., Chandra, G., Jakimowicz, D., Yuqing, T., Bruton, C.J. and Chater, K.F. (2004) Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv. Appl. Microbiol., 54, 107-128.
32. Schwedock, J., McCormick, J.R., Angert, E.R., Nodwell, J.R. and Losick, R. (1997) Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor. Mol. Microbiol., 25, 847-858.
33. Jyothikumar, V., Klanbut, K., Tiong, J., Roxburgh, J.S., Hunter, I.S., Smith, T.K. and Herron, P.R. (2012) Cardiolipin synthase is required for Streptomyces coelicolor morphogenesis. Mol. Microbiol., 84, 181-197.
34. Otwinowski,Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr., 276(Pt A), 307-326.
35. Kissinger, C.R., Gehlhaar, D.K. and Fogel, D.B. (1999) Rapid automated molecular replacement by evolutionary search. Acta. Crystallogr. D Biol. Crystallogr., 55, 484-491.
36. Langer, G., Cohen, S.X., Lamzin, V.S. and Perrakis, A. (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc., 3, 1171-1179.
37. Emsley,P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta. Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
38. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta. Crystallogr. D Biol. Crystallogr., 53, 240-255.
39. McGhee, J.D. and von Hippel, P.H. (1974) Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J. Mol. Biol., 86, 469-489.
40. Klotz, I.M. (1997) Ligand-receptor energetics:a guide for the perplexed. Wiley, New York.
41. Heichlinger, A., Ammelburg, M., Kleinschnitz, E.M., Latus, A., Maldener, I., Flardh, K., Wohlleben,W. and Muth, G. (2011) The MreB-like protein Mbl of Streptomyces coelicolor A3(2) depends on MreB for proper localization and contributes to spore wall synthesis. J. Bacteriol., 193, 1533-1542.
42. Pei,J. and Grishin, N.V. (2007) PROMALS: towards accurate multiple sequence alignments of distantly related proteins. Bioinformatics, 23, 802-808.
43. Abascal, F., Zardoya,R. and Posada, D. (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics, 21, 2104-2105.
44. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk,W. and Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol., 59, 307-321.
45. Anisimova,M. and Gascuel, O. (2006) Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst. Biol., 55, 539-552.
46. Gouy, M., Guindon,S. and Gascuel, O. (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol., 27, 221-224.
47. Marintcheva, B., Marintchev, A., Wagner,G. and Richardson, C.C. (2008) Acidic C-terminal tail of the ssDNA-binding protein of bacteriophage T7 and ssDNA compete for the same binding surface. Proc. Natl Acad. Sci. USA, 105, 1855-1860.
48. Bratlie, M.S., Johansen, J., Sherman, B.T., Huang da, W., Lempicki, R.A. and Drablos, F. (2010) Gene duplications in prokaryotes can be associated with environmental adaptation. BMC Genomics, 11, 588.
49. Jakimowicz, D., Mouz, S., Zakrzewska-Czerwinska,J. and Chater, K.F. (2006) Developmental control of a parAB promoter leads to formation of sporulation-associated ParB complexes in Streptomyces coelicolor. J. Bacteriol., 188, 1710-1720.
50. Ryding, N.J., Bibb, M.J., Molle, V., Findlay, K.C., Chater, K.F. and Buttner, M.J. (1999) New sporulation loci in Streptomyces coelicolor A3(2). J. Bacteriol., 181, 5419-5425.
51. Ainsa, J.A., Ryding, N.J., Hartley, N., Findlay, K.C., Bruton, C.J. and Chater, K.F. (2000) WhiA, a protein of unknown function conserved among gram-positive bacteria, is essential for sporulation in Streptomyces coelicolor A3(2). J. Bacteriol., 182, 5470-5478.
52. Bourn, W.R. and Babb, B. (1995) Computer assisted identification and classification of streptomycete promoters. Nucleic Acids Res., 23, 3696-3703.
53. Strohl, W.R. (1992) Compilation and analysis of DNA sequences associated with apparent streptomycete promoters. Nucleic Acids Res., 20, 961-974.
54. Ahel, I., Vujaklija, D., Mikoc,A. and Gamulin, V. (2002) Transcriptional analysis of the recA gene in Streptomyces rimosus: identification of the new type of promoter. FEMS Microbiol. Lett., 209, 133-137.
55. Krissinel,E. and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta. Crystallogr. D Biol. Crystallogr., 60, 2256-2268.
56. Krissinel,E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol., 372, 774-797.
57. Stefanic, Z., Vujaklija, D., Andrisic, L., Mikleusevic, G., Andrejasic, M., Turk,D. and Luic, M. (2007) Preliminary crystallographic study of Streptomyces coelicolor single-stranded DNA-binding protein. Croatica. Chemica. Acta., 80, 35-39.
58. Noens, E.E., Mersinias, V., Traag, B.A., Smith, C.P., Koerten, H.K. and van Wezel, G.P. (2005) SsgA-like proteins determine the fate of peptidoglycan during sporulation of Streptomyces coelicolor. Mol. Microbiol., 58, 929-944.
59. Flardh, K., Findlay, K.C. and Chater, K.F. (1999) Association of early sporulation genes with suggested developmental decision points in Streptomyces coelicolor A3(2). Microbiology, 145(Pt 9), 2229-2243.
60. Kang, J.G., Paget, M.S., Seok, Y.J., Hahn, M.Y., Bae, J.B., Hahn, J.S., Kleanthous, C., Buttner, M.J. and Roe, J.H. (1999) RsrA, an anti-sigma factor regulated by redox change. EMBO J., 18, 4292-4298.
61. Lohman, T.M. and Ferrari, M.E. (1994) Escherichia coli single-stranded DNA-binding protein: multiple DNA-binding modes and cooperativities. Annu. Rev. Biochem., 63, 527-570.
62. Kozlov, A.G., Cox, M.M. and Lohman, T.M. (2010) Regulation of single-stranded DNA binding by the C termini of Escherichia coli single-stranded DNA-binding (SSB) protein. J. Biol. Chem., 285, 17246-17252.
63. Zhi, X.Y., Li, W.J. and Stackebrandt, E. (2009) An update of the structure and 16S rRNA gene sequence-based definition of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and emended descriptions of the existing higher taxa. Int. J. Syst. Evol. Microbiol., 59, 589-608.
64. Gust, B., Challis, G.L., Fowler, K., Kieser,T. and Chater, K.F. (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl Acad. Sci. USA, 100, 1541-1546.
65. Gregory, M.A., Till,R. and Smith, M.C. (2003) Integration site for Streptomyces phage phiBT1 and development of site-specific integrating vectors. J. Bacteriol., 185, 5320-5323.
66. DeSanti, C.L. and Strohl, W.R. (2003) Characterization of the Streptomyces sp. strain C5 snp locus and development of snp-derived expression vectors. Appl. Environ. Microbiol., 69, 1647-1654.
67. MacNeil, D.J., Gewain, K.M., Ruby, C.L., Dezeny, G., Gibbons, P.H. and MacNeil, T. (1992) Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene, 111, 61-68.
68. Cherepanov, P.P. and Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene, 158, 9-14.