One of the two genes encoding nucleoid-associated HU proteins in Streptomyces coelicolor is developmentally regulated and specifically involved in spore maturation

Journal of Bacteriology

Volumn 191, Issue 21, 2009, Pages 6489-6500

  Salerno, Paola ^a,c   Larsson, Jessica ^a   Bucca, Giselda ^b   Laing, Emma ^b   Smith, Colin P ^b   Flärdh, Klas ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF SURREY   (United Kingdom)

^c SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HU PROTEIN; LYSINE;

ARTICLE; BACTERIAL SPORE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA MICROARRAY; EUKARYOTE; FUNGUS HYPHAE; GENE DELETION; HEAT TOLERANCE; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PHYLUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPOROGENESIS; STREPTOMYCES COELICOLOR; UPREGULATION; VEGETATIVE STAGE;

BACTERIAL PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; SPORES, BACTERIAL; STREPTOMYCES COELICOLOR;

ACTINOBACTERIA; EUKARYOTA; MYCOBACTERIUM SMEGMATIS; STREPTOMYCES; STREPTOMYCES COELICOLOR; STREPTOMYCINEAE;

EID: 70350462621     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00709-09     Document Type: Article

References (54)

1. Aínsa, J. A., H. D. Parry, and K. F. Chater. 1999. A response regulator-like protein that functions at an intermediate stage of sporulation in Streptomyces coelicolor A3(2). Mol. Microbiol. 34:607-619.
2. Almiron, M., A. J. Link, D. Furlong, and R. Kolter. 1992. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6:2646-2654. (Pubitemid 23052891)
3. Ausmees, N., H. Wahlstedt, S. Bagchi, M. A. Elliot, M. J. Buttner, and K. Flärdh. 2007. SmeA, a small membrane protein with multiple functions in Streptomyces sporulation including targeting of a SpoIIIE/FtsK-like protein to cell division septa. Mol. Microbiol. 65:1458-1473.
4. Azam, T. A., A. Iwata, A. Nishimura, S. Ueda, and A. Ishihama. 1999. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181:6361-6370.
5. Bentley, S. D., K. F. Chater, A. M. Cerdeno-Tarraga, G. L. Challis, N. R. Thomson, K. D. James, D. E. Harris, M. A. Quail, H. Kieser, D. Harper, A. Bateman, S. Brown, G. Chandra, C. W. Chen, M. Collins, A. Cronin, A. Fraser, A. Goble, J. Hidalgo, T. Hornsby, S. Howarth, C. H. Huang, T. Kieser, L. Larke, L. Murphy, K. Oliver, S. O'Neil, E. Rabbinowitsch, M. A. Rajandream, K. Rutherford, S. Rutter, K. Seeger, D. Saunders, S. Sharp, R. Squares, S. Squares, K. Taylor, T. Warren, A. Wietzorrek, J. Woodward, B. G. Barrell, J. Parkhill, and D. A. Hopwood. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147.
6. Bierman, M., R. Logan, K. O'Brien, E. T. Seno, R. N. Rao, and B. E. Schoner. 1992. Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116:43-49.
7. Blondelet-Rouault, M.-H., J. Weiser, A. Lebrihi, P. Branny, and J.-L. Pernodet. 1997. Antibiotic resistance gene cassettes derived from the Ω interposon for use in E. coli and Streptomyces. Gene 190:315-317. (Pubitemid 27220139)
8. Bourn, W. R., and B. Babb. 1995. Computer assisted identification and classification of streptomycete promoters. Nucleic Acids Res. 23:3696-3703.
9. Chater, K. F., and G. Chandra. 2006. The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol. Rev. 30:651-672.
10. Chen, J. M., H. Ren, J. E. Shaw, Y. J. Wang, M. Li, A. S. Leung, V. Tran, N. M. Berbenetz, D. Kocincova, C. M. Yip, J. M. Reyrat, and J. Liu. 2008. Lsr2 of Mycobacterium tuberculosis is a DNA-bridging protein. Nucleic Acids Res. 36:2123-2135.
11. Churchill, M. E., and A. A. Travers. 1991. Protein motifs that recognize structural features of DNA. Trends Biochem. Sci. 16:92-97.
12. Dedrick, R. M., H. Wildschutte, and J. R. McCormick. 2009. Genetic interactions of smc, ftsK, and parB genes in Streptomyces coelicolor and their developmental genome segregation phenotypes. J. Bacteriol. 191:320-332.
13. Elliot, M. A., M. J. Buttner, and J. R. Nodwell. 2008. Multicellular development of Streptomyces, p. 419-438. In D. E. Whitworth (ed.), Myxobacteria. Multicellularity and differentiation. ASM Press, Washington, DC.
14. Ensign, J. C. 1978. Formation, properties, and germination of actinomycete spores. Annu. Rev. Microbiol. 32:185-219.
15. Flärdh, K. 2003. Growth polarity and cell division in Streptomyces. Curr. Opin. Microbiol. 6:564-571.
16. Flärdh, K., and M. J. Buttner. 2009. Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat. Rev. Microbiol. 7:36-49.
17. Flärdh, K., K. C. Findlay, and K. F. Chater. 1999. Association of early sporulation genes with suggested developmental decision points in Streptomyces coelicolor A3(2). Microbiology 145:2229-2243.
18. Flärdh, K., E. Leibovitz, M. J. Buttner, and K. F. Chater. 2000. Generation of a non-sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter. Mol. Microbiol. 38:737-749.
19. Frenkiel-Krispin, D., I. Ben-Avraham, J. Englander, E. Shimoni, S. G. Wolf, and A. Minsky. 2004. Nucleoid restructuring in stationary-state bacteria. Mol. Microbiol. 51:395-405.
20. Ghosh, S., and A. Grove. 2006. The Deinococcus radiodurans-encoded HU protein has two DNA-binding domains. Biochemistry 45:1723-1733.
21. Guo, F., and S. Adhya. 2007. Spiral structure of Escherichia coli HUαβ provides foundation for DNA supercoiling. Proc. Natl. Acad. Sci. USA 104:4309-4314.
22. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
23. Jakimowicz, D., S. Mouz, J. Zakrzewska-Czerwinska, and K. F. Chater. 2006. Developmental control of a parAB promoter leads to formation of sporulation-associated ParB complexes in Streptomyces coelicolor. J. Bacteriol. 188:1710-1720. (Pubitemid 43346850)
24. Jakimowicz, D., P. Zydek, A. Kois, J. Zakrzewska-Czerwinska, and K. F. Chater. 2007. Alignment of multiple chromosomes along helical ParA scaffolding in sporulating Streptomyces hyphae. Mol. Microbiol. 65:625-641.
25. Janssen, G. R., and M. J. Bibb. 1993. Derivatives of pUC18 that have BglII sites flanking a modified multiple cloning site and that retain the ability to identify recombinant clones by visual screening of Escherichia coli colonies. Gene 124:133-134. (Pubitemid 23065980)
26. Kasinsky, H. E., J. D. Lewis, J. B. Dacks, and J. Ausio. 2001. Origin of H1 linker histones. FASEB J. 15:34-42.
27. Kelemen, G. H., P. Brian, K. Flärdh, L. C. Chamberlin, K. F. Chater, and M. J. Buttner. 1998. Developmental regulation of transcription of whiE, a locus specifying the polyketide spore pigment in Streptomyces coelicolor A3(2). J. Bacteriol. 180:2515-2521.
28. Kelemen, G. H., G. L. Brown, J. Kormanec, L. Potúcková, K. F. Chater, and M. J. Buttner. 1996. The positions of the sigma factor genes whiG and sigF in the hierarchy controlling the development of spore chains in the aerial hyphae of Streptomyces coelicolor A3(2). Mol. Microbiol. 21:593-603.
29. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces genetics. The John Innes Foundation, Norwich, United Kingdom.
30. Kois, A., M. Swiatek, D. Jakimowicz, and J. Zakrzewska-Czerwinska. 2009. SMC protein-dependent chromosome condensation during aerial hyphal development in Streptomyces. J. Bacteriol. 191:310-319.
31. Lee, B. H., B. Murugasu-Oei, and T. Dick. 1998. Upregulation of a histone-like protein in dormant Mycobacterium smegmatis. Mol. Gen. Genet. 260:475-479.
32. Lee, K. S., D. Bumbaca, J. Kosman, P. Setlow, and M. J. Jedrzejas. 2008. Structure of a protein-DNA complex essential for DNA protection in spores of Bacillus species. Proc. Natl. Acad. Sci. USA 105:2806-2811.
33. Luijsterburg, M. S., M. C. Noom, G. J. Wuite, and R. T. Dame. 2006. The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: a molecular perspective. J. Struct. Biol. 156:262-272.
34. Luijsterburg, M. S., M. F. White, R. van Driel, and R. T. Dame. 2008. The major architects of chromatin: architectural proteins in bacteria, archaea and eukaryotes. Crit. Rev. Biochem. Mol. Biol. 43:393-418.
35. Mattimore, V., and J. R. Battista. 1996. Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J. Bacteriol. 178:633-637.
36. Mazza, P., E. E. Noens, K. Schirner, N. Grantcharova, A. M. Mommaas, H. K. Koerten, G. Muth, K. Flärdh, G. P. van Wezel, and W. Wohlleben. 2006. MreB of Streptomyces coelicolor is not essential for vegetative growth but is required for the integrity of aerial hyphae and spores. Mol. Microbiol. 60:838-852.
37. Molle, V., W. J. Palframan, K. C. Findlay, and M. J. Buttner. 2000. WhiD and WhiB, homologous proteins required for different stages of sporulation in Steptomyces coelicolor A3(2). J. Bacteriol. 182:1286-1295.
38. Mukherjee, A., G. Bhattacharyya, and A. Grove. 2008. The C-terminal domain of HU-related histone-like protein Hlp from Mycobacterium smegmatis mediates DNA end-joining. Biochemistry 47:8744-8753.
39. Mukherjee, A., P. J. DiMario, and A. Grove. 2009. Mycobacterium smegmatis histone-like protein Hlp is nucleoid associated. FEMS Microbiol. Lett. 291:232-240.
40. Nair, S., and S. E. Finkel. 2004. Dps protects cells against multiple stresses during stationary phase. J. Bacteriol. 186:4192-4198. (Pubitemid 38802567)
41. Paull, T. T., and R. C. Johnson. 1995. DNA looping by Saccharomyces cerevisiae high mobility group proteins NHP6A/B. Consequences for nucleoprotein complex assembly and chromatin condensation. J. Biol. Chem. 270:8744-8754.
42. Phillips, R. W., J. Wiegel, C. J. Berry, C. Fliermans, A. D. Peacock, D. C. White, and L. J. Shimkets. 2002. Kineococcus radiotolerans sp. nov., a radiation-resistant, gram-positive bacterium. Int. J. Syst. Evol. Microbiol. 52:933-938.
43. F, is required for the late stages of morphological differentiation in Streptomyces spp. Mol. Microbiol. 17:37-48.
44. Prabhakar, S., P. S. Annapurna, N. K. Jain, A. B. Dey, J. S. Tyagi, and H. K. Prasad. 1998. Identification of an immunogenic histone-like protein (HLPMt) of Mycobacterium tuberculosis. Tuber. Lung Dis. 79:43-53.
45. Redenbach, M., H. M. Kieser, D. Denapaite, A. Eichner, J. Cullum, H. Kinashi, and D. A. Hopwood. 1996. A set of ordered cosmids and a detailed genetic and physical map of the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol. Microbiol. 21:77-96.
46. Roque, A., I. Iloro, I. Ponte, J. L. Arrondo, and P. Suau. 2005. DNA-induced secondary structure of the carboxyl-terminal domain of histone H1. J. Biol. Chem. 280:32141-32147.
47. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Setlow, P. 2007. I will survive: DNA protection in bacterial spores. Trends Microbiol. 15:172-180. (Pubitemid 46528251)
49. Shires, K., and L. Steyn. 2001. The cold-shock stress response in Mycobacterium smegmatis induces the expression of a histone-like protein. Mol. Microbiol. 39:994-1009.
50. Thanbichler, M., and L. Shapiro. 2006. Chromosome organization and segregation in bacteria. J. Struct. Biol. 156:292-303.
51. Ventura, M., C. Canchaya, A. Tauch, G. Chandra, G. F. Fitzgerald, K. F. Chater, and D. van Sinderen. 2007. Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol. Mol. Biol. Rev. 71:495-548.
52. Wang, L., Y. Yu, X. He, X. Zhou, Z. Deng, K. F. Chater, and M. Tao. 2007. Role of an FtsK-like protein in genetic stability in Streptomyces coelicolor A3(2). J. Bacteriol. 189:2310-2318.
53. Yokoyama, E., K. Doi, M. Kimura, and S. Ogata. 2001. Disruption of the hup gene encoding a histone-like protein HS1 and detection of HS12 of Streptomyces lividans. Res. Microbiol. 152:717-723.
54. Zimmerman, S. B. 2006. Shape and compaction of Escherichia coli nucleoids. J. Struct. Biol. 156:255-261.