Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1991 Nov;173(21):6849–6858. doi: 10.1128/jb.173.21.6849-6858.1991

Genetic organization and regulation of the xylose degradation genes in Streptomyces rubiginosus.

H C Wong 1, Y Ting 1, H C Lin 1, F Reichert 1, K Myambo 1, K W Watt 1, P L Toy 1, R J Drummond 1
PMCID: PMC209037  PMID: 1657868

Abstract

The xylose isomerase (xylA) and the xylulose kinase (xylB) genes from Streptomyces rubiginosus were isolated, and their nucleotide sequences were determined. The xylA and xylB genes encode proteins of 388 and 481 amino acids, respectively. These two genes are transcribed divergently from within a 114-nucleotide sequence separating the coding regions. Regulation of the xyl genes in S. rubiginosus was examined by fusing their promoters to the Pseudomonas putida catechol dioxygenase gene and integrating the fusions into the minicircle integration site on the S. rubiginosus chromosome. The expression of catechol dioxygenase was then measured under a variety of conditions. The results indicated that transcription of the xyl genes was induced by D-xylose and repressed by glucose. Data from quantitative S1 mapping were consistent with this conclusion and suggested that xylA had one and xylB had two transcription initiation sites. The transcription initiation site of xylA was 40 bp upstream of the coding region. The two transcription initiation sites of xylB were 20 and 41 bp 5' of its translation initiation codon. Under control of appropriate regulatory elements, the cloned xyl genes are capable of complementing either Escherichia coli xylose isomerase- or xylulose kinase-deficient strains. The deduced amino acid sequence of the S. rubiginosus xylA protein is highly homologous to sequences of other microbial xylose isomerases.

Full text

PDF
6849

Images in this article

6851FIG. 1
on p.6851
6854FIG. 4
on p.6854

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  2. Bibb M. J., Cohen S. N. Gene expression in Streptomyces: construction and application of promoter-probe plasmid vectors in Streptomyces lividans. Mol Gen Genet. 1982;187(2):265–277. doi: 10.1007/BF00331128. [DOI] [PubMed] [Google Scholar]
  3. Bibb M. J., Findlay P. R., Johnson M. W. The relationship between base composition and codon usage in bacterial genes and its use for the simple and reliable identification of protein-coding sequences. Gene. 1984 Oct;30(1-3):157–166. doi: 10.1016/0378-1119(84)90116-1. [DOI] [PubMed] [Google Scholar]
  4. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bolivar F., Rodriguez R. L., Betlach M. C., Boyer H. W. Construction and characterization of new cloning vehicles. I. Ampicillin-resistant derivatives of the plasmid pMB9. Gene. 1977;2(2):75–93. doi: 10.1016/0378-1119(77)90074-9. [DOI] [PubMed] [Google Scholar]
  6. Brauer A. W., Oman C. L., Margolies M. N. Use of o-phthalaldehyde to reduce background during automated Edman degradation. Anal Biochem. 1984 Feb;137(1):134–142. doi: 10.1016/0003-2697(84)90359-2. [DOI] [PubMed] [Google Scholar]
  7. Carrell H. L., Rubin B. H., Hurley T. J., Glusker J. P. X-ray crystal structure of D-xylose isomerase at 4-A resolution. J Biol Chem. 1984 Mar 10;259(5):3230–3236. [PubMed] [Google Scholar]
  8. Chater K. F., Hopwood D. A., Kieser T., Thompson C. J. Gene cloning in Streptomyces. Curr Top Microbiol Immunol. 1982;96:69–95. doi: 10.1007/978-3-642-68315-2_5. [DOI] [PubMed] [Google Scholar]
  9. David J. D., Wiesmeyer H. Control of xylose metabolism in Escherichia coli. Biochim Biophys Acta. 1970 Mar 24;201(3):497–499. doi: 10.1016/0304-4165(70)90171-6. [DOI] [PubMed] [Google Scholar]
  10. Drocourt D., Bejar S., Calmels T., Reynes J. P., Tiraby G. Nucleotide sequence of the xylose isomerase gene from Streptomyces violaceoniger. Nucleic Acids Res. 1988 Oct 11;16(19):9337–9337. doi: 10.1093/nar/16.19.9337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Farber G. K., Petsko G. A., Ringe D. The 3.0 A crystal structure of xylose isomerase from Streptomyces olivochromogenes. Protein Eng. 1987 Dec;1(6):459–466. doi: 10.1093/protein/1.6.459. [DOI] [PubMed] [Google Scholar]
  12. GROSS E., WITKOP B. Nonenzymatic cleavage of peptide bonds: the methionine residues in bovine pancreatic ribonuclease. J Biol Chem. 1962 Jun;237:1856–1860. [PubMed] [Google Scholar]
  13. Ghangas G. S., Wilson D. B. Isolation and characterization of the Salmonella typhimurium LT2 xylose regulon. J Bacteriol. 1984 Jan;157(1):158–164. doi: 10.1128/jb.157.1.158-164.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gritz L., Davies J. Plasmid-encoded hygromycin B resistance: the sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccharomyces cerevisiae. Gene. 1983 Nov;25(2-3):179–188. doi: 10.1016/0378-1119(83)90223-8. [DOI] [PubMed] [Google Scholar]
  15. Grunstein M., Wallis J. Colony hybridization. Methods Enzymol. 1979;68:379–389. doi: 10.1016/0076-6879(79)68027-8. [DOI] [PubMed] [Google Scholar]
  16. Gärtner D., Geissendörfer M., Hillen W. Expression of the Bacillus subtilis xyl operon is repressed at the level of transcription and is induced by xylose. J Bacteriol. 1988 Jul;170(7):3102–3109. doi: 10.1128/jb.170.7.3102-3109.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Henrick K., Blow D. M., Carrell H. L., Glusker J. P. Comparison of backbone structures of glucose isomerase from Streptomyces and Arthrobacter. Protein Eng. 1987 Dec;1(6):467–469. doi: 10.1093/protein/1.6.467. [DOI] [PubMed] [Google Scholar]
  18. Henrick K., Collyer C. A., Blow D. M. Structures of D-xylose isomerase from Arthrobacter strain B3728 containing the inhibitors xylitol and D-sorbitol at 2.5 A and 2.3 A resolution, respectively. J Mol Biol. 1989 Jul 5;208(1):129–157. doi: 10.1016/0022-2836(89)90092-2. [DOI] [PubMed] [Google Scholar]
  19. Hentschel C., Irminger J. C., Bucher P., Birnstiel M. L. Sea urchin histone mRNA termini are located in gene regions downstream from putative regulatory sequences. Nature. 1980 May 15;285(5761):147–151. doi: 10.1038/285147a0. [DOI] [PubMed] [Google Scholar]
  20. Hewick R. M., Hunkapiller M. W., Hood L. E., Dreyer W. J. A gas-liquid solid phase peptide and protein sequenator. J Biol Chem. 1981 Aug 10;256(15):7990–7997. [PubMed] [Google Scholar]
  21. Kirby K. S., Fox-Carter E., Guest M. Isolation of deoxyribonucleic acid and ribosomal ribonucleic acid from bacteria. Biochem J. 1967 Jul;104(1):258–262. doi: 10.1042/bj1040258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  23. Lawlis V. B., Dennis M. S., Chen E. Y., Smith D. H., Henner D. J. Cloning and sequencing of the xylose isomerase and xylulose kinase genes of Escherichia coli. Appl Environ Microbiol. 1984 Jan;47(1):15–21. doi: 10.1128/aem.47.1.15-21.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lee C. Y., Bagdasarian M., Meng M. H., Zeikus J. G. Catalytic mechanism of xylose (glucose) isomerase from Clostridium thermosulfurogenes. Characterization of the structural gene and function of active site histidine. J Biol Chem. 1990 Nov 5;265(31):19082–19090. [PubMed] [Google Scholar]
  25. Lessie T. G., Whiteley H. R. Properties of threonine deaminase from a bacterium able to use threonine as sole source of carbon. J Bacteriol. 1969 Nov;100(2):878–889. doi: 10.1128/jb.100.2.878-889.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lydiate D. J., Ikeda H., Hopwood D. A. A 2.6 kb DNA sequence of Streptomyces coelicolor A3(2) which functions as a transposable element. Mol Gen Genet. 1986 Apr;203(1):79–88. doi: 10.1007/BF00330387. [DOI] [PubMed] [Google Scholar]
  27. Maleszka R., Wang P. Y., Schneider H. A Col E1 hybrid plasmid containing Escherichia coli genes complementing d-xylose negative mutants of Escherichia coli and Salmonella typhimurium. Can J Biochem. 1982 Feb;60(2):144–151. doi: 10.1139/o82-020. [DOI] [PubMed] [Google Scholar]
  28. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  29. McLaughlin J. R., Wong H. C., Ting Y. E., Van Arsdell J. N., Chang S. Control of lysogeny and immunity of Bacillus subtilis temperate bacteriophage SP beta by its d gene. J Bacteriol. 1986 Sep;167(3):952–959. doi: 10.1128/jb.167.3.952-959.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Meselson M., Yuan R. DNA restriction enzyme from E. coli. Nature. 1968 Mar 23;217(5134):1110–1114. doi: 10.1038/2171110a0. [DOI] [PubMed] [Google Scholar]
  31. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  32. Mills D. R., Kramer F. R. Structure-independent nucleotide sequence analysis. Proc Natl Acad Sci U S A. 1979 May;76(5):2232–2235. doi: 10.1073/pnas.76.5.2232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Mizusawa S., Nishimura S., Seela F. Improvement of the dideoxy chain termination method of DNA sequencing by use of deoxy-7-deazaguanosine triphosphate in place of dGTP. Nucleic Acids Res. 1986 Feb 11;14(3):1319–1324. doi: 10.1093/nar/14.3.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Moran C. P., Jr, Lang N., Losick R. Nucleotide sequence of a Bacillus subtilis promoter recognized by Bacillus subtilis RNA polymerase containing sigma 37. Nucleic Acids Res. 1981 Nov 25;9(22):5979–5990. doi: 10.1093/nar/9.22.5979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Piszkiewicz D., Landon M., Smith E. L. Anomalous cleavage of aspartyl-proline peptide bonds during amino acid sequence determinations. Biochem Biophys Res Commun. 1970 Sep 10;40(5):1173–1178. doi: 10.1016/0006-291x(70)90918-6. [DOI] [PubMed] [Google Scholar]
  36. Rosenberg S. A., Grimm E. A., McGrogan M., Doyle M., Kawasaki E., Koths K., Mark D. F. Biological activity of recombinant human interleukin-2 produced in Escherichia coli. Science. 1984 Mar 30;223(4643):1412–1414. doi: 10.1126/science.6367046. [DOI] [PubMed] [Google Scholar]
  37. Rosenfeld S. A., Stevis P. E., Ho N. W. Cloning and characterization of the xyl genes from Escherichia coli. Mol Gen Genet. 1984;194(3):410–415. doi: 10.1007/BF00425552. [DOI] [PubMed] [Google Scholar]
  38. Saari G. C., Kumar A. A., Kawasaki G. H., Insley M. Y., O'Hara P. J. Sequence of the Ampullariella sp. strain 3876 gene coding for xylose isomerase. J Bacteriol. 1987 Feb;169(2):612–618. doi: 10.1128/jb.169.2.612-618.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sarthy A. V., McConaughy B. L., Lobo Z., Sundstrom J. A., Furlong C. E., Hall B. D. Expression of the Escherichia coli xylose isomerase gene in Saccharomyces cerevisiae. Appl Environ Microbiol. 1987 Sep;53(9):1996–2000. doi: 10.1128/aem.53.9.1996-2000.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Schellenberg G. D., Sarthy A., Larson A. E., Backer M. P., Crabb J. W., Lidstrom M., Hall B. D., Furlong C. E. Xylose isomerase from Escherichia coli. Characterization of the protein and the structural gene. J Biol Chem. 1984 Jun 10;259(11):6826–6832. [PubMed] [Google Scholar]
  42. Seno E. T., Chater K. F. Glycerol catabolic enzymes and their regulation in wild-type and mutant strains of Streptomyces coelicolor A3(2). J Gen Microbiol. 1983 May;129(5):1403–1413. doi: 10.1099/00221287-129-5-1403. [DOI] [PubMed] [Google Scholar]
  43. Shamanna D. K., Sanderson K. E. Genetics and regulation of D-xylose utilization in Salmonella typhimurium LT2. J Bacteriol. 1979 Jul;139(1):71–79. doi: 10.1128/jb.139.1.71-79.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985 Oct;150(1):76–85. doi: 10.1016/0003-2697(85)90442-7. [DOI] [PubMed] [Google Scholar]
  45. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  46. Staden R. An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res. 1982 May 11;10(9):2951–2961. doi: 10.1093/nar/10.9.2951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  48. Virolle M. J., Bibb M. J. Cloning, characterization and regulation of an alpha-amylase gene from Streptomyces limosus. Mol Microbiol. 1988 Mar;2(2):197–208. doi: 10.1111/j.1365-2958.1988.tb00021.x. [DOI] [PubMed] [Google Scholar]
  49. Whitlow M., Howard A. J., Finzel B. C., Poulos T. L., Winborne E., Gilliland G. L. A metal-mediated hydride shift mechanism for xylose isomerase based on the 1.6 A Streptomyces rubiginosus structures with xylitol and D-xylose. Proteins. 1991;9(3):153–173. doi: 10.1002/prot.340090302. [DOI] [PubMed] [Google Scholar]
  50. Wilhelm M., Hollenberg C. P. Nucleotide sequence of the Bacillus subtilis xylose isomerase gene: extensive homology between the Bacillus and Escherichia coli enzyme. Nucleic Acids Res. 1985 Aug 12;13(15):5717–5722. doi: 10.1093/nar/13.15.5717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Wilhelm M., Hollenberg C. P. Selective cloning of Bacillus subtilis xylose isomerase and xylulokinase in Escherichia coli genes by IS5-mediated expression. EMBO J. 1984 Nov;3(11):2555–2560. doi: 10.1002/j.1460-2075.1984.tb02173.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wong H. C., Schnepf H. E., Whiteley H. R. Transcriptional and translational start sites for the Bacillus thuringiensis crystal protein gene. J Biol Chem. 1983 Feb 10;258(3):1960–1967. [PubMed] [Google Scholar]
  53. Woo S. L. A sensitive and rapid method for recombinant phage screening. Methods Enzymol. 1979;68:389–395. doi: 10.1016/0076-6879(79)68028-x. [DOI] [PubMed] [Google Scholar]
  54. Wovcha M. G., Steuerwald D. L., Brooks K. E. Amplification of D-xylose and D-glucose isomerase activities in Escherichia coli by gene cloning. Appl Environ Microbiol. 1983 Apr;45(4):1402–1404. doi: 10.1128/aem.45.4.1402-1404.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Yang R., Lis J., Wu R. Elution of DNA from agarose gels after electrophoresis. Methods Enzymol. 1979;68:176–182. doi: 10.1016/0076-6879(79)68012-6. [DOI] [PubMed] [Google Scholar]
  56. Zoller M. J., Smith M. Oligonucleotide-directed mutagenesis of DNA fragments cloned into M13 vectors. Methods Enzymol. 1983;100:468–500. doi: 10.1016/0076-6879(83)00074-9. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES