Skip to main content
SpringerLink
Log in

The use of the rare UUA codon to define “Expression Space” for genes involved in secondary metabolism, development and environmental adaptation in Streptomyces

  • Review
  • Published:
The Journal of Microbiology Aims and scope Submit manuscript

Abstract

In Streptomyces coelicolor, bldA encodes the only tRNA for a rare leucine codon, UUA. This tRNA is unnecessary for growth, but is required for some aspects of secondary metabolism and morphological development, as revealed by the phenotypes of bldA mutants in diverse streptomycetes. This article is a comprehensive review of out understanding of this unusual situation. Based on information from four sequenced genomes it now appears that, typically, about 2–3% of genes in any one streptomycete contain a TTA codon, most having been acquired through species-specific horizontal gene transfer. Among the few widely conserved TTA-containing genes, mutations in just one, the pleiotropic regulatory gene adpA, give an obvious phenotype: such mutants are defective in aerial growth and sporulation, but vary in the extent of their impairment in secondary metabolism in different streptomycetes. The TTA codon in adpA is largely responsible for the morphological phenotype of a bldA mutant of S. coelicolor. AdpA-dependent targets include several genes involved in the integrated action of extracellular proteases that, at least in some species, are involved in the conversion of primary biomass into spores. The effects of bldA mutations on secondary metabolism are mostly attributable to the presence of TTA codons in pathway-specific genes, particularly in transcriptional activator genes. This is not confined to S. coelicolor — it is true for about half of all known antibiotic biosynthetic gene sets from streptomycetes. Combined microarray and proteomic analysis of liquid (and therefore non-sporulating) S. coelicolor bldA mutant cultures revealed effects of the mutation during rapid growth, during transition phase, and in stationary phase. Some of these effects may be secondary consequences of changes in the pattern of ppGpp accumulation. It is argued that the preferential accumulation of the bldA tRNA under conditions in which growth is significantly constrained has evolved to favour the expression of genes that confer adaptive benefits in intermittently encountered sub-optimal environments. The evolution of this system may have been a secondary consequence of the selective pressure exerted by bacteriophage attack. Some biotechnological implications of bldA phenomenology are considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bentley, S.D., S. Brown, L.D. Murphy, D.E. Harris, M.A. Quail, J. Parkhill, B.G. Barrell, J.R. McCormick, R.I. Santamaria, R. Losick, M. Yamasaki, H. Kinashi, C.W. Chen, G. Chandra, D. Jakimowicz, H.M. Kieser, T. Kieser, and K.F. Chater. 2004. SCP1, a 356,023 bp linear plasmid adapted to the ecology and developmental biology of its host, Streptomyces coelicolor A3(2). Mol. Microbiol. 51, 1615–1628.

    Article  PubMed  CAS  Google Scholar 

  • 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, et al. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141–147.

    Article  PubMed  Google Scholar 

  • Bruton, C.J., E.P. Guthrie, and K.F. Chater. 1991. Phage vectors that allow monitoring of transcription of secondary metabolism genes in Streptomyces. Biotechnology 9, 652–656.

    Article  PubMed  CAS  Google Scholar 

  • Chakraburtty, R. and M. Bibb. 1997. The ppGpp synthetase gene (relA) of Streptomyces coelicolor A3(2) plays a conditional role in antibiotic production and morphological differentiation. J. Bacteriol. 179, 5854–5861.

    PubMed  CAS  Google Scholar 

  • Champness, W.C. 1988. New loci required for Streptomyces coelicolor morphological and physiological differentiation. J. Bacteriol. 170, 1168–1174.

    PubMed  CAS  Google Scholar 

  • Champness, W.C. and K.F. Chater. 1994. The regulation and interaction of antibiotic production and morphological differentiation in Streptomyces spp. In P. Piggot, C. Moran, and P. Youngman. (eds.), Regulation of bacterial differentiation. Washington, American Society for Microbiology, 6193.

    Google Scholar 

  • Chater, K.F. 2001. Regulation of sporulation in Streptomyces coelicolor A3(2): a checkpoint multiplex? Curr. Opin. Microbiol. 4, 667–673.

    Article  PubMed  CAS  Google Scholar 

  • Chater, K.F. 2006. Streptomyces inside out: a new perspective on the bacteria that provide us with antibiotics. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 361, 761–768.

    Article  CAS  Google Scholar 

  • Chater, K.F. and G. Chandra. 2006. The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol. Rev. 30, 651–672.

    Article  PubMed  CAS  Google Scholar 

  • Chater, K.F. and S. Horinouchi. 2003. Signalling early developmental events in two highly diverged Streptomyces species. Mol. Microbiol. 48, 9–15.

    Article  PubMed  CAS  Google Scholar 

  • Crick, F. 1966. Codon-anticodon pairing: the wobble hypothesis. J. Mol. Biol. 19, 548–555.

    PubMed  CAS  Google Scholar 

  • Distler, J., K. Mansouri, G. Mayer, M. Stockmann, and W. Piepersberg. 1992. Streptomycin biosynthesis and its regulation in streptomycetes. Gene 115, 105–111.

    Article  PubMed  CAS  Google Scholar 

  • Elliot, M. and N.J. Talbot. 2004. Building filaments in the air: aerial morphogenesis in bacteria and fungi. Curr. Opin. Microbiol. 7, 594–601.

    Article  PubMed  CAS  Google Scholar 

  • Eustaquio, A.S., B. Gust, U. Galm, S.M. Li, K.F. Chater, and L. Heide. 2005. Heterologous expression of novobiocin and clorobiocin biosynthetic gene clusters. Appl. Environ. Microbiol. 71, 2452–2459.

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Moreno, M.A., J.L. Caballero, D.A. Hopwood, and F. Malpartida. 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.

    Article  PubMed  CAS  Google Scholar 

  • Fuglsang, A. 2005. Intragenic position of UUA codons in streptomycetes. Microbiology 151, 3150–3152.

    Article  PubMed  CAS  Google Scholar 

  • Gehring, A., J. Nodwell, S. Beverley, and R. Losick. 2000. Genomewide insertional mutagenesis in Streptomyces coelicolor reveals additional genes involved in morphological differentiation. Proc. Natl. Acad. Sci. USA 97, 9642–9647.

    Article  PubMed  CAS  Google Scholar 

  • Gramajo, H.C., E. Takano, and M.J. Bibb. 1993. Stationary phase production of the antibiotic actinorhodin in Streptomyces coelicolor is transcriptionally regulated. Mol. Microbiol. 7, 837–845.

    Article  PubMed  CAS  Google Scholar 

  • Guthrie, E.P. and K.F. Chater. 1990. The level of a transcript required for production of a Streptomyces coelicolor antibiotic is conditionally dependent on a tRNA gene. J. Bacteriol. 172, 6189–6193.

    PubMed  CAS  Google Scholar 

  • Guthrie, E.P., C.S. Flaxman, J. White, D.A. Hodgson, M.J. Bibb, and K.F. Chater. 1998. A response-regulator-like activator of antibiotic synthesis from Streptomyces coelicolor A3(2) with an amino-terminal domain that lacks a phosphorylation pocket. Microbiology 144, 727–738.

    PubMed  CAS  Google Scholar 

  • Hesketh, A., G. Bucca, E. Laing, F. Flett, G. Hotchkiss, C.P. Smith, and K.F. Chater. 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.

    Article  PubMed  CAS  Google Scholar 

  • Hirano, S., J. Kato, Y. Ohnishi, and S. Horinouchi. 2006. Control of the Streptomyces subtilisin inhibitor gene by AdpA in the A-factor regulatory cascade in Streptomyces griseus. J. Bacteriol. 188, 6207–6216.

    Article  PubMed  CAS  Google Scholar 

  • Hopwood, D. 1967. Genetic analysis and genome structure in Streptomyces coelicolor. Bacteriol. Rev. 31, 373–403.

    PubMed  CAS  Google Scholar 

  • Horinouchi, S. 2002. A microbial hormone, A-factor, as a master switch for morphological differentiation and secondary metabolism in Streptomyces griseus. Front. Biosci. 7, D2045–D2057.

    Article  PubMed  CAS  Google Scholar 

  • Ikeda, H., J. Ishikawa, A. Hanamoto, M. Shinose, H. Kikuchi, T. Shiba, Y. Sakaki, M. Hattori, and S. Omura. 2003. Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat. Biotechnol. 21, 526–531.

    Article  PubMed  Google Scholar 

  • Jayapal, K.P., W. Lian, F. Glod, and W.S. Hu. 2007. Comparative genome hybridizations reveal absence of large Streptomyces coelicolor genomic islands in Streptomyces lividans. BMC Genomics 8, 229.

    Article  PubMed  CAS  Google Scholar 

  • Kataoka, M., S. Kosono, and G. Tsujimoto. 1999. Spatial and temporal regulation of protein expression by bldA within a Streptomyces lividans colony. FEBS Lett. 462, 425–429.

    Article  PubMed  CAS  Google Scholar 

  • Kato, J., A. Suzuki, H. Yamazaki, Y. Ohnishi, and S. Horinouchi. 2002. Control by A-factor of a metalloendopeptidase gene involved in aerial mycelium formation in Streptomyces griseus. J. Bacteriol. 184, 6016–6025.

    Article  PubMed  CAS  Google Scholar 

  • Kato, J.Y., I. Miyahisa, M. Mashiko, Y. Ohnishi, and S. Horinouchi. 2004. A single target is sufficient to account for the biological effects of the A-factor receptor protein of Streptomyces griseus. J. Bacteriol. 186, 2206–2211.

    Article  PubMed  CAS  Google Scholar 

  • Kato, J.Y., W.J. Chi, Y. Ohnishi, S.K. Hong, and S. Horinouchi. 2005a. Transcriptional control by A-factor of two trypsin genes in Streptomyces griseus. J. Bacteriol. 187, 286–295.

    Article  PubMed  CAS  Google Scholar 

  • Kato, J.Y., Y. Ohnishi, and S. Horinouchi. 2005b. Autorepression of AdpA of the AraC/XylS family, a key transcriptional activator in the A-factor regulatory cascade in Streptomyces griseus. J. Mol. Biol. 350, 12–26.

    Article  PubMed  CAS  Google Scholar 

  • Kelemen, G.H. and M.J. Buttner. 1999. Initiation of aerial mycelium formation in Streptomyces. Curr. Opin. Microbiol. 2, 106–106(1).

    Article  Google Scholar 

  • Kim, I. and K.J. Lee. 1995. Physiological roles of leupeptin and extracellular proteases in mycelium development of Streptomyces exfoliatus SMF13. Microbiology 141, 1017–1025.

    PubMed  CAS  Google Scholar 

  • Kim, D.-W., K. Chater, K.-J. Lee, and A. Hesketh. 2005a. 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.

    Article  PubMed  CAS  Google Scholar 

  • Kim, D.-W., K. Chater, K.J. Lee, and A. Hesketh. 2005b. Effects of growth phase and the developmentally significant bldA-specified tRNA on the membrane-associated proteome of Streptomyces coelicolor. Microbiology 151, 2707–2720.

    Article  PubMed  CAS  Google Scholar 

  • Kodani, S., M.E. Hudson, M.C. Durrant, M.J. Buttner, J.R. Nodwell, and J.M. Willey. 2004. The SapB morphogen is a lantibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor. Proc. Natl. Acad. Set USA 101, 11448–11453.

    Article  CAS  Google Scholar 

  • Kwak, J., L.A. McCue, and K.E. Kendrick. 1996. Identification of bldA mutants of Streptomyces griseus. Gene 171, 75–78.

    Article  PubMed  CAS  Google Scholar 

  • Lautru, S., R.J. Deeth, L.M. Bailey, and G.L. Challis. 2005. Discovery of a new peptide natural product by Streptomyces coelicolor genome mining. Nat. Chem. Biol. 1, 265–269.

    Article  PubMed  CAS  Google Scholar 

  • Lawlor, E.J., H.A. Baylis, and K.F. Chater. 1987. Pleiotropic morphological and antibiotic deficiencies result from mutations in a gene encoding a transfer RNA-like product in Streptomyces coelicolor A3(2). Genes Dev. 1, 1305–1310.

    Article  PubMed  CAS  Google Scholar 

  • Leskiw, B.K., E.J. Lawlor, J.M. FernandezAbalos, and K.F. Chater. 1991a. TTA codons in some genes prevent their expression in a class of developmental, antibiotic-negative, Streptomyces mutants. Proc. Natl. Acad. Sci. USA 88, 24612465.

    Article  Google Scholar 

  • Leskiw, B.K., M.J. Bibb, and K.F. Chater. 1991b. The use of a rare codon specifically during development? Mol. Microbiol. 5, 2861–2867.

    Article  PubMed  CAS  Google Scholar 

  • Leskiw, B.K., R. Mah, E.J. Lawlor, and K.F. Chater. 1993. Accumulation of bldA-specified tRNA is temporally regulated in Streptomyces coelicolor A3(2). J. Bacteriol. 175, 1995–2005.

    PubMed  CAS  Google Scholar 

  • Li, W., J. Wu, W. Tao, C. Zhao, Y. Wang, X. He, G. Chandra, X. Zhou, Z. Deng, K.F. Chater, and M. Tao. 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.

    Article  PubMed  CAS  Google Scholar 

  • Manteca, A., M. Fernandez, and J. Sanchez. 2006. Cytological and biochemical evidence for an early cell dismantling event in surface cultures of Streptomyces antibioticus. Res. Microbiol. 157, 143–152.

    Article  PubMed  CAS  Google Scholar 

  • Merrick, M. 1976. A morphological and genetic mapping study of bald colony mutants of Streptomyces coelicolor. J. Gen. Microbiol. 96, 299–315.

    PubMed  CAS  Google Scholar 

  • Nguyen, K.T., J. Tenor, H. Stettler, L.T. Nguyen, L.D. Nguyen, and C.J. Thompson. 2003. Colonial differentiation in Streptomyces coelicolor depends on translation of a specific codon within the adpA gene. J. Bacteriol. 185, 7291–7296.

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi, Y., S. Kameyama, H. Onaka, and S. Horinouchi. 1999. The A-factor regulatory cascade leading to streptomycin biosynthesis in Streptomyces griseus: identification of a target gene of the A-factor receptor. Mol. Microbiol. 34, 102–111.

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi, Y., H. Yamazaki, J.Y. Kato, A. Tomono, and S. Horinouchi. 2005. AdpA, a central transcriptional regulator in the A-factor regulatory cascade that leads to morphological development and secondary metabolism in Streptomyces griseus. Biosci. Biotechnol. Biochem. 69, 431–439.

    Article  PubMed  CAS  Google Scholar 

  • O’Rourke, S. 2003. Regulation of methylenomycin biosynthesis. Ph. D. thesis, University of East Anglia, Norwich, UK.

    Google Scholar 

  • Passantino, R., A.M. Puglia, and K.F. Chater. 1991. Additional copies of the actII regulatory gene induce actinorhodin production in pleiotropic bld mutants of Streptomyces coelicolor A3(2). J. Gen. Microbiol. 137, 20592064.

    Google Scholar 

  • Perez-Llarena, F.J., P. Liras, A. Rodriguez-Garcia, and J.F. Martin. 1997. A regulatory gene (ccaR) required for cephamycin and clavulanic acid production in Streptomyces clavuligerus: amplification results in overproduction of both beta-lactam compounds. J. Bacteriol. 179, 2053–2059.

    PubMed  CAS  Google Scholar 

  • Piret, J.M. and K.F. Chater. 1985. Phage-mediated cloning of bldA, a region involved in Streptomyces coelicolor morphological development, and its analysis by genetic complementation. J. Bacteriol. 163, 965–972.

    PubMed  CAS  Google Scholar 

  • Rebets, Y.V., B.O. Ostash, M. Fukuhara, T. Nakamura, and V.O. Fedorenko. 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.

    Article  PubMed  CAS  Google Scholar 

  • Rozenski, J., P.F. Crain, and J.A. McCloskey. 1999. The RNA modification database: 1999 update. Nucleic Acids Res. 27, 196–197.

    Article  PubMed  CAS  Google Scholar 

  • Song, L., F. Barona-Gomez, C. Corre, L. Xiang, D.W. Udwary, M.B. Austin, J.P. Noel, B.S. Moore, and G.L. Challis. 2006. Type III polyketide synthase β-ketoacyl-ACP starter unit and ethylmalonyl-CoA extender unit selectivity discovered by Streptomyces coelicolor genome mining. J. Am. Chem. Soc. 128, 14754–14755.

    Article  PubMed  CAS  Google Scholar 

  • Strauch, E., E. Takano, H.A. Baylis, and M.J. Bibb. 1991. The stringent response in Streptomyces coelicolor A3(2). Mol. Microbiol. 5, 289–298.

    Article  PubMed  CAS  Google Scholar 

  • Takano, E., M. Tao, F. Long, M.J. Bibb, L. Wang, W. Li, M.J. Buttner, Z.X. Deng, and K.F. Chater. 2003. A rare leucine codon in adpA is implicated in the morphological defect of bldA mutants of Streptomyces coelicolor. Mol. Microbiol. 50, 475–486.

    Article  PubMed  CAS  Google Scholar 

  • Tao, W.F., J. Wu, Z.X. Deng, and M.F. Tao. 2007. Cloning of bldAa and the effect on morphological differentiation and avermectins production in Streptomyces avermitilis NRRL8165. Wei Sheng Wu Xue Bao (In Chinese) 47, 34–38.

    CAS  Google Scholar 

  • Tercero, J.A., J.C. Espinosa, and A. Jimenez. 1998. Expression of the Streptomyces alboniger pur cluster in Streptomyces lividans is dependent on the bldA-encoded tRNALeu. FEBS Lett. 421, 221–223.

    Article  PubMed  CAS  Google Scholar 

  • Tomono, A., Y. Tsai, Y. Ohnishi, and S. Horinouchi. 2005. Three chymotrypsin genes are members of the AdpA regulon in the A-factor regulatory cascade in Streptomyces griseus. J. Bacteriol. 187, 6341–6353.

    Article  PubMed  CAS  Google Scholar 

  • Trepanier, N.K., S. Jensen, D.C. Alexander, and B.K. Leskiw. 2002. The positive activator of cephamycin C and clavulanic acid production in Streptomyces clavuligerus is mistranslated in a bldA mutant. Microbiology 148, 643–656.

    PubMed  CAS  Google Scholar 

  • Trepanier, N.K., G.D. Nguyen, P.J. Leedell, and B.K. Leskiw. 1997. Use of polymerase chain reaction to identify a leucyl tRNA in Streptomyces coelicolor. Gene 193, 59–63.

    Article  PubMed  CAS  Google Scholar 

  • Ueda, K., K.I. Oinuma, G. Ikeda, K. Hosono, Y. Ohnishi, S. Horinouchi, and T. Beppu. 2002. AmfS, an extracellular peptidic morphogen in Streptomyces griseus. J. Bacteriol. 184, 1488–1492.

    Article  PubMed  CAS  Google Scholar 

  • Ueda, K., H. Takano, M. Nishimoto, H. Inaba, and T. Beppu. 2005. Dual transcriptional control of amfTSBA, which regulates the onset of cellular differentiation in Streptomyces griseus. J. Bacteriol. 187, 135–142.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Vohradsky, J. and C.J. Thompson. 2006. Systems level analysis of protein synthesis patterns associated with bacterial growth and metabolic transitions. Proteomics 6, 785–793.

    Article  PubMed  CAS  Google Scholar 

  • White, J. and M. Bibb. 1997. bldA dependence of undecylprodigiosin production in Streptomyces coelicolor A3(2) involves a pathway-specific regulatory cascade. J. Bacteriol. 179, 627–633.

    PubMed  CAS  Google Scholar 

  • Widdick, D.A., H.M. Dodd, P. Barraille, J. White, T.H. Stein, K.F. Chater, M.J. Gasson, and M.J. Bibb. 2003. Cloning and engineering of the cinnamycin biosynthetic gene cluster from Streptomyces cinnamoneus cinnamoneus DSM 40005. Proc. Natl. Acad. Sci. USA 100, 4316–4321.

    Article  PubMed  CAS  Google Scholar 

  • Willey, J., J. Schwedock, and R. Losick. 1993. Multiple extracellular signals govern the production of a morphogenetic protein involved in aerial mycelium formation by Streptomyces coelicolor. Genes Dev. 7, 895–903.

    Article  PubMed  CAS  Google Scholar 

  • Willey, J., A. Willems, S. Kodani, and J.R. Nodwell. 2006. Morphogenetic surfactants and their role in the formation of aerial hyphae in Streptomyce coelicolor. Mol. Microbiol. 59, 731–742.

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki, H., Y. Ohnishi, and S. Horinouchi. 2000. An A-factor-dependent extracytoplasmic function sigma factor [oAdsA] that is essential for morphological development in Streptomyces griseus. J. Bacteriol. 182, 4596–4605.

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki, H., A. Takano, Y. Ohnishi, and S. Horinouchi. 2003a. amfR, an essential gene for aerial mycelium formation, is a member of the AdpA regulon in the A-factor regulatory cascade in Streptomyces griseus. Mol. Microbiol. 50, 1173–1187.

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki, H., Y. Ohnishi, and S. Horinouchi. 2003b. Transcriptional switch-on by A-factor of ssgA that is essential for spore septum formation in Streptomyces griseus. J. Bacteriol. 285, 1273–1283.

    Article  CAS  Google Scholar 

  • Yamazaki, H., A. Tomono, Y. Ohnishi, and S. Horinouchi. 2004. DNA-binding specificity of AdpA, a transcriptional activator in the A-factor regulatory cascade in Streptomyces griseus. Mol. Microbiol. 53, 555–572.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Microbiology, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK

    Keith F. Chater & Govind Chandra

Authors
  1. Keith F. Chater
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Govind Chandra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Keith F. Chater.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chater, K.F., Chandra, G. 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 (2008). https://doi.org/10.1007/s12275-007-0233-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-007-0233-1

Keywords

Search

Navigation