tRNA accumulation and suppression of the bldA phenotype during development in Streptomyces coelicolor

Molecular Microbiology

Volumn 79, Issue 6, 2011, Pages 1602-1614

  Pettersson, B M Fredrik ^a   Kirsebom, Leif A ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYSTEINE; LEUCINE; RIBONUCLEASE P; TRANSFER RNA; URACIL;

ANTICODON; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOACCUMULATION; BLDA GENE; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA PROCESSING; STREPTOMYCES COELICOLOR;

BASE SEQUENCE; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PHENOTYPE; RNA, BACTERIAL; RNA, TRANSFER; RNA, TRANSFER, LEU; STREPTOMYCES COELICOLOR;

STREPTOMYCES COELICOLOR;

EID: 79952380621     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07543.x     Document Type: Article

References (43)

1. Bentley, S.D., Chater, K.F., Cerdeño-Tárraga, A.M., Challis, G.L., Thomson, N.R., James, K.D., etal. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147.
2. Bentley, S.D., Brown, S., Murphy, L.D., Harris, D.E., Quail, M.A., Parkhill, J., etal. (2004) SCP1, a 356023bp linear plasmid adapted to the ecology and developmental biology of its host, Streptomyces coelicolor A3(2). Mol Microbiol 51: 1615-1628.
3. Bierman, M., Logan, R., O'Brien, K., Seno, E.T., Rao, R.N., and Schoner, B.E. (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116: 43-49.
4. Chandra, G., and Chater, K.F. (2008) Evolutionary flux of potentially bldA-dependent Streptomyces genes containing the rare leucine codon TTA. Antonie Van Leeuwenhoek 94: 111-126.
5. Chater, K.F., and Chandra, G. (2006) The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol Rev 30: 651-672.
6. Chater, K.F., and Chandra, G. (2008) The use of the rare UUA codon to define 'expression space' for genes involved in secondary metabolism, development and environmental adaptation in Streptomyces. J Microbiol 46: 1-11.
7. Chater, K.F., Bruton, C.J., King, A.A., and Suarez, J.E. (1982) The expression of Streptomyces and Escherichia coli drug-resistance determinants cloned into the Streptomyces phage phi C31. Gene 19: 21-32.
8. Church, G.M., and Gilbert, W. (1984) Genomic sequencing. Proc Natl Acad Sci USA 81: 1991-1995.
9. Claessen, D., de Jong, W., Dijkhuizen, L., and Wösten, H.A. (2006) Regulation of Streptomyces development: reach for the sky! Trends Microbiol 14: 313-319.
10. Fernández-Moreno, M.A., Caballero, J.L., Hopwood, D.A., and Malpartida, F. (1991) The act cluster contains regulatory and antibiotic export genes, direct targets for translational control by the bldA tRNA gene of Streptomyces. Cell 66: 769-780.
11. Gopalan, V., and Altman, S. (2006) Ribonuclease P: structure and catalysis. In The RNA World, 3rd edn. Gesteland, R.F., Cech, T.R., and Atkins, J.F. (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press [WWW document]. URL
12. Gramajo, H.C., Takano, E., and Bibb, M.J. (1993) Stationary-phase production of the antibiotic actinorhodin in Streptomyces coelicolor A3(2) is transcriptionally regulated. Mol Microbiol 7: 837-845.
13. Hesketh, A., Bucca, G., Laing, E., Flett, F., Hotchkiss, G., Smith, C.P., and Chater, K.F. (2007) New pleiotropic effects of eliminating a rare tRNA from Streptomyces coelicolor, revealed by combined proteomic and transcriptomic analysis of liquid cultures. BMC Genomics 8: 261.
14. Hopwood, D.A. (1999) Forty years of genetics with Streptomyces: from in vivo through in vitro to in silico. Microbiology 145: 2183-2202.
15. Hopwood, D.A., Bibb, M.J., Chater, K.F., Kieser, T., Bruton, C.J., Kieser, H.M., etal. (1985) Genetic Manipulation of Streptomyces: A Laboratory Manual. Norwich, UK: The John Innes Foundation.
16. Kataoka, M., Kosono, S., and Tsujimoto, G. (1999) Spatial and temporal regulation of protein expression by bldA within a Streptomyces lividans colony. FEBS Lett 462: 425-429.
17. Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., and Hopwood, D.A. (2000) Practical Streptomyces Genetics. Norwich, UK: The John Innes Foundation.
18. Kim, D.W., Chater, K.F., Lee, K.J., and Hesketh, A. (2005a) Effects of growth phase and the developmentally significant bldA-specified tRNA on the membrane-associated proteome of Streptomyces coelicolor. Microbiology 151: 2707-2720.
19. Kim, D.W., Chater, K., Lee, K.J., and Hesketh, A. (2005b) Changes in the extracellular proteome caused by the absence of the bldA gene product, a developmentally significant tRNA, reveal a new target for the pleiotropic regulator AdpA in Streptomyces coelicolor. J Bacteriol 187: 2957-2966.
20. Kirsebom, L.A. (2007) RNase P RNA mediated cleavage: substrate recognition and catalysis. Biochimie 89: 1183-1194.
21. Kirsebom, L.A., and Trobro, S. (2009) RNase P RNA-mediated cleavage. IUBMB Life 61: 189-200.
22. Lai, L.B., Vioque, A., Kirsebom, L.A., and Gopalan, V. (2010) Unexpected diversity of RNase P, an ancient tRNA processing enzyme: challenges and prospects. FEBS Lett 584: 287-296.
23. Lawlor, E.J., Baylis, H.A., and Chater, K.F. (1987) Pleiotropic morphological and antibiotic deficiencies result from mutations in a gene encoding a tRNA-like product in Streptomyces coelicolor A3(2). Genes Dev 1: 1305-1310.
24. Leskiw, B.K., Bibb, M.J., and Chater, K.F. (1991a) The use of a rare codon specifically during development? Mol Microbiol 5: 2861-2867.
25. Leskiw, B.K., Lawlor, E.J., Fernandez-Abalos, J.M., and Chater, K.F. (1991b) TTA codons in some genes prevent their expression in a class of developmental, antibiotic-negative, Streptomyces mutants. Proc Natl Acad Sci USA 88: 2461-2465.
26. Leskiw, B.K., Mah, R., Lawlor, E.J., and Chater, K.F. (1993) Accumulation of bldA-specified tRNA is temporally regulated in Streptomyces coelicolor A3(2). J Bacteriol 175: 1995-2005.
27. Li, W., Wu, J., Tao, W., Zhao, C., Wang, Y., He, X., etal. (2007) A genetic and bioinformatic analysis of Streptomyces coelicolor genes containing TTA codons, possible targets for regulation by a developmentally significant tRNA. FEMS Microbiol Lett 266: 20-28.
28. Li, Y., Cole, K., and Altman, S. (2003) The effect of a single, temperature-sensitive mutation on global gene expression in Escherichia coli. RNA 9: 518-532.
29. 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.
30. Nguyen, K.T., Tenor, J., Stettler, H., Nguyen, L.T., Nguyen, L.D., and Thompson, C.J. (2003) Colonial differentiation in Streptomyces coelicolor depends on translation of a specific codon within the adpA gene. J Bacteriol 185: 7291-7296.
31. Paget, M.S., Chamberlin, L., Atrih, A., Foster, S.J., and Buttner, M.J. (1999) Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2). J Bacteriol 181: 204-211.
32. Pettersson, B.M.F., and Kirsebom, L.A. (2008) The presence of a C-1/G+73 pair in a tRNA precursor influences processing and expression in vivo. J Mol Biol 381: 1089-1097.
33. Rebets, Y.V., Ostash, B.O., Fukuhara, M., Nakamura, T., and Fedorenko, V.O. (2006) Expression of the regulatory protein LndI for landomycin E production in Streptomyces globisporus 1912 is controlled by the availability of tRNA for the rare UUA codon. FEMS Microbiol Lett 256: 30-37.
34. Sarkar, S., Azad, A.K., and Hopper, A.K. (1999) Nuclear tRNA aminoacylation and its role in nuclear export of endogenous tRNAs in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 96: 14366-14371.
35. Takai, K., Horie, N., Yamaizumi, Z., Nishimura, S., Miyazawa, T., and Yokoyama, S. (1994) Recognition of UUN codons by two leucine tRNA species from Escherichia coli. FEBS Lett 344: 31-34.
36. Takano, E., Tao, M., Long, F., Bibb, M.J., Wang, L., Li, W., etal. (2003) A rare leucine codon in adpA is implicated in the morphological defect of bldA mutants of Streptomyces coelicolor. Mol Microbiol 50: 475-486.
37. Tang, T.-H., Polacek, N., Zywicki, M., Huber, H., Brugger, K., Garrett, R., etal. (2005) Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus. Mol Microbiol 55: 469-481.
38. Trepanier, N.K., Nguyen, G.D., Leedell, P.J., and Leskiw, B.K. (1997) Use of polymerase chain reaction to identify a leucyl tRNA in Streptomyces coelicolor. Gene 193: 59-63.
39. Trepanier, N.K., Jensen, S.E., Alexander, D.C., and Leskiw, B.K. (2002) The positive activator of cephamycin C and clavulanic acid production in Streptomyces clavuligerus is mistranslated in a bldA mutant. Microbiology 148: 643-656.
40. Ueda, Y., Kumagai, I., and Miura, K. (1992) The effects of a unique D-loop structure of a minor tRNA(UUALeu) from Streptomyces on its structural stability and amino acid accepting activity. Nucleic Acids Res 20: 3911-3917.
41. White, J., and Bibb, M. (1997) bldA dependence of undecylprodigiosin production in Streptomyces coelicolor A3(2) involves a pathway-specific regulatory cascade. J Bacteriol 179: 627-633.
42. Wildermuth, H., and Hopwood, D.A. (1970) Septation during sporulation in Streptomyces coelicolor. J Gen Microbiol 60: 51-59.
43. Willkomm, D.K., Minnerup, J., Hüttenhofer, A., and Hartmann, R.K. (2005) Experimental RNomics in Aquifex aeolicus: identification of small non-coding RNAs and the putative 6S RNA homolog. Nucleic Acids Res 33: 1949-1960.