Cloning and analysis of the spinosad biosynthetic gene cluster of Saccharopolyspora spinosa

Chemistry and Biology

Volumn 8, Issue 5, 2001, Pages 487-499

  Waldron, Clive ^a   Matsushima, Patti ^b   Rosteck Jr , Paul R ^b   Broughton, Mary C ^b   Turner, Jan ^b   Madduri, Krishnamurthy ^a   Crawford, Kathryn P ^a   Merlo, Donald J ^a   Baltz, Richard H ^a,b  

^a DOW AGROSCIENCES LLC   (United States)

^b ELI LILLY AND COMPANY   (United States)

Author keywords

Glycosylation; Macrolide; Polyketide biosynthesis; Saccharopolyspora spinosa; Spinosad; Spinosyn

Indexed keywords

BIOCHEMICAL PATHWAY; ENZYME SUBUNIT; FOROSAMINE; GENE CLUSTER; GENE DISRUPTION; GENETIC TRANSFORMATION; MACROLIDE; METHYLATION; MOLECULAR CLONING; MOLECULAR SIZE; OPEN READING FRAME; POLYKETIDE SYNTHASE; RHAMNOSE; SECONDARY METABOLITE; SPINOSAD; SPINOSYN A; SYNTHETIC DNA;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; DRUG COMBINATIONS; HEXOSAMINES; MACROLIDES; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; OPEN READING FRAMES; RHAMNOSE; SACCHAROPOLYSPORA;

ACTINOBACTERIA (CLASS); INSECTA; SACCHAROPOLYSPORA SPINOSA;

EID: 0035017135     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-5521(01)00029-1     Document Type: Article

References (62)

1. H.A. Kirst, K.H. Michel, J.W. Martin, L.C. Creemer, E.H. Chio, R.C. Yao, W.M. Nakatsukasa, L. Boeck, J.L. Occolowitz, J.W. Paschal, J.B. Deeter, N.D. Jones, G.D. Thompson, A83543A-D, unique fermentation-derived tetracyclic macrolides, Tetrahedron Lett. 32 (1991) 4839-4842.
2. H.A. Kirst, K.H. Michel, J.S. Mynderse, E.H. Chio, R.C. Yao, W.M. Nakatsukasa, L. Boeck, J.L. Occolowitz, J.W. Paschal, J.B. Deeter, G.D. Thompson, Discovery, isolation, and structure elucidation of a family of structurally unique, fermentation-derived tetracyclic macrolides, in: D.R. Baker, J.G. Fenyes, J.J. Steffens (Eds.), Synthesis and Chemistry of Agrochemicals III, American Chemical Society, Washington, DC, 1992, pp. 214-225.
3. F.P. Mertz, R.C. Yao, Saccharopolyspora spinosa sp. nov. isolated from soil collected in a sugar mill rum still, Int. J. Syst. Bacteriol. 40 (1990) 34-39.
4. C.V. DeAmicis, J.E. Dripps, C.J. Hatten, L. Karr, Physical and biological properties of the spinosyns: novel macrolide pest-control agents from fermentation, in: P.A. Hedin, R.M. Hollingworth, E.P. Masler, J. Miyamoto, D.G. Thompson (Eds.), ACS Symposium Series 658: Phytochemicals for Pest Control, American Chemical Society, Washington, DC, 1997, pp. 144-154.
5. T.C. Sparks, G.D. Thompson, H.A. Kirst, M.B. Hertline, L.L. Larson, T.V. Worden, S.T. Thibault, Biological activity of the spinosyns, new fermentation derived insect control agents, on tobacco budworm (Lepidoptera: Nocuidae) larvae, J. Econ. Entomol. 91 (1998) 1277-1283.
6. G.D. Crouse, T.C. Sparks, Naturally derived materials as products and leads for insect control: the spinosyns, Rev. Toxicol. 2 (1998) 133-146.
7. T.C. Sparks, G.D. Thompson, H.A. Kirst, M.B. Hertlein, J.S. Mynderse, J.R. Turner, T.V. Worden, Fermentation-derived insect control agents: the spinosyns, Methods Biotechnol. 5 (1999) 171-188.
8. S. Donadio, M.J. Staver, J.B. McAlpine, S.J. Swanson, L. Katz, Modular organization of genes required for complex polyketide biosynthesis, Science 252 (1991) 675-679.
9. H. Ikeda, T. Nomoniya, M. Usami, T. Ohta, S. Omura, Organization of the biosynthetic gene cluster of the polyketide anthelmintic macrolide avermectin in Streptomyces avermitilis, Proc. Natl. Acad. Sci. USA 96 (1999) 9509-9514.
10. T. Schwecke, J.F. Aparicio, I. Molnar, A. Konig, L.E. Khaw, S.F. Haydock, M. Oliynnnk, P. Caffrey, J. Cortes, J.B. Lester, G.A. Bohm, J. Staunton, P.F. Leadlay, The biosynthetic gene cluster for the polyketide immunosuppressant rapamycin, Proc. Natl. Acad. Sci. USA 92 (1995) 7839-7843.
11. D. Cane, C.C. Yang, Nargenicin biosynthesis: late stage oxidations and absolute configuration, J. Antibiot. 38 (1984) 423-426.
12. P.R. Graupner, S. Thornburgh, J.T. Mathieson, E.L. Chapin, G.M. Kemmit, J.M. Brown, C.E. Snipes, Dihydromaltophilin; a novel fungicidal tetramic acid containing metabolite from Streptomyces sp., J. Antibiot. 50 (1997) 1014-1091.
13. P. Matsushima, M.C. Broughton, J.R. Turner, R.H. Baltz, Conjugal transfer of cosmid DNA from Escherichia coli to Saccharopolyspora spinosa: effects of chromosomal insertions on macrolide production, Gene 146 (1994) 39-45.
14. P. Matsushima, R.H. Baltz, Transformation of Saccharopolyspora spinosa protoplasts with plasmid DNA modified in vitro to avoid host restriction, Microbiology 140 (1994) 139-143.
15. R.H. Baltz, Genetic manipulation of antibiotic-producing Streptomyces, Trends Microbiol. 6 (1998) 76-83.
16. M. Basinski, M. Bierman, B. Schoner, Cloning of polyketide biosynthetic genes using colony hybridization and PCR, Dev. Indust. Microbiol. 33 (1993) 237-241.
17. M. Bierman, R. Logan, K. O'Brien, E.T. Seno, R.N. Rao, B.E. Schoner, Plasmid cloning vectors for the transfer of DNA from Escherichia coli to Streptomyces spp., Gene 116 (1992) 43-49.
18. S.F. Altschul, W. Gish, W. Miller, W. Myers, D.J. Lipman, Basic local alignment search tool, J. Mol. Biol. 251 (1990) 403-410.
19. W.R. Pearson, Rapid and sensitive sequence comparison with FASTP and FASTA, Methods Enzymol. 183 (1990) 63-98.
20. C. Bisang, P.F. Long, J. Cortes, J. Westcott, J. Crosby, A.-L. Matharu, R.J. Cox, T.J. Simmpson, J. Staunton, P.F. Leadlay, A chain initiation factor common to both modular and aromatic polyketide synthases, Nature 401 (1999) 502-505.
21. S.F. Haydock, J.F. Aparicio, I. Molnar, T. Schwecke, L.E. Khaw, A. Konig, A.F. Marsden, I.S. Galloway, J. Staunton, P.F. Leadlay, Divergent sequence motifs correlated with the substrate specificity of (methyl)malonyl-CoA:acyl carrier protein transacylase domains in modular polyketide synthases, FEBS Lett. 374 (1995) 246-248.
22. S.J. Kakavas, L. Katz, D. Stassi, Identification and characterization of the niddamycin polyketide synthase genes from Streptomyces caelestis, J. Bacteriol. 179 (1997) 7515-7522.
23. I. Molnar, T. Schupp, M. Ono, R.E. Zirkle, M. Milnamoow, B. Nowak-Thompspon, N. Engle, C. Toupet, A. Stratmann, D.D. Cyr, J. Gorlach, J.M. Mayo, A. Hu, S. Goff, J. Schmid, J.M. Ligon, The biosynthetic gene cluster for the microtubule-stabilizing agents epothilones A and B from Sorangium cellulosum So ce90, Chem. Biol. 7 (2000) 97-109.
24. B. Julian, S. Shah, R. Ziermann, R. Goldman, L. Katz, C. Khosla, Isolation and characterization of the epothilone biosynthetic gene cluster from Sorangium cellulosum, Gene 249 (2000) 153-160.
25. A. Trefzer, J.A. Salas, A. Bechthold, Genes and enzymes involved in deoxysugar biosynthesis, Nat. Prod. Rep. 16 (1999) 283-299.
26. L. Katz, Manipulation of modular polyketide synthases, Chem. Rev. 97 (1997) 2557-2575.
27. K. Ichinose, D.J. Bedford, D. Tornus, A. Bechthold, M.J. Bibb, W.P. Revill, H.G. Floss, D.A. Hopwood, The granaticin biosynthetic gene cluster of Streptomyces violaceoruber Tu22: sequence analysis and expression in a heterologous host, Chem. Biol. 5 (1998) 647-659.
28. L.A. Mershon-Davies, E. Cundliffe, Analysis of five tylosin biosynthetic genes from the tylIBA region of the Streptomyces fradiae genome, Mol. Microbiol. 13 (1994) 349-355.
29. N. Bate, E. Cundliffe, The mycinose-biosynthetic genes of Streptomyces fradiae, producer of tylosin, J. Indust. Microbiol. Biotechnol. 23 (1999) 118-122.
30. R. Fouces, E. Mellado, B. Diez, J.L. Barredo, The tylosin biosynthetic cluster from Streptomyces fradiae: genetic organization of the left region, Microbiology 145 (1999) 855-868.
31. L. Westrich, S. Domann, B. Faust, D. Bedford, D.A. Hopwood, A. Bechthold, Cloning and characterization of a gene cluster from Streptomyces cyanogenus S136 probably involved in landomycin biosynthesis, FEMS Microbiol. Lett. 170 (1999) 381-387.
32. G. Draeger, S.-H. Park, H.G. Floss, Mechanism of the 2-deoxygenation step in the biosynthesis of the deoxyhexose moieties of the antibiotics granaticin and oleandomycin, J. Am. Chem. Soc. 121 (1998) 2611-2612.
33. A.M.A. van Wageningen, P.N. Kiekpatrick, D.H. Williams, B.R. Harris, J.K. Kershaw, N.J. Lennard, M. Jones, S.J. Jones, P.J. Solenberg, Sequencing and analysis of genes involved in the biosynthesis of a vancomycin group antibiotic, Chem. Biol. 5 (1998) 155-162.
34. J.S. Thorson, S.F. Lo, H.-W. Liu, C.R. Hutchinson, Biosynthesis of 3,6-dideoxyhexoses: new mechanistic reflections upon 2,6-dideoxy, and amino sugar construction, J. Am. Chem. Soc. 115 (1993) 6993-6994.
35. U. Peschke, H. Schmidt, H.-Z. Zhang, W. Piepersberg, Molecular characterization of the lincomycin-production gene cluster of Streptomyces lincolnensis 78-11, Mol. Microbiol. 16 (1995) 1137-1156.
36. W. Piepersberg, Molecular biology, biochemistry, and fermentation of aminoglycoside antibiotics, in: W. Strohl (Ed.), Biotechnology of Antibiotics, Marcel Dekker, Inc., New York, 1997, pp. 81-163.
37. Y. Xue, L. Zhao, H.W. Liu, D.H. Sherman, A gene cluster for macrolide antibiotic biosynthesis in Streptomyces venezuelae: architecture of metabolic diversity, Proc. Natl. Acad. Sci. USA 95 (1998) 12111-12116.
38. E. Cundliffe, S.A. Fish, V.T.W. Wilson, A. Gandecha, S.L. Large, Glycosyl transfer during tylosin production in Streptomyces fradiae, Dev. Indust. Microbiol. 34 (1997) 109-114.
39. S.A. Fish, E. Cundliffe, Stimulation of polyketide metabolism in Streptomyces fradiae by tylosin and its glycosylated precursors, Microbiology 143 (1997) 3871-3876.
40. R.H. Baltz, E.T. Seno, Genetics of Streptomyces fradiae and tylosin biosynthesis, Ann. Rev. Microbiol. 42 (1988) 547-574.
41. A.A.R. Gandecha, S.L. Large, E. Cundliffe, Analysis of four tylosin biosynthetic genes from the tylLM region of the Streptomyces fradiae genome, Gene 184 (1997) 197-203.
42. Y. Mao, M. Varoglu, D.H. Sherman, Molecular characterization and analysis of the biosynthetic gene cluster for the antitumor antibiotic mitomycin C from Streptomyces lavendulae NRRL 2564, Chem. Biol. 6 (1999) 251-263.
43. P.R. August, L. Tang, Y.J. Yoon, S. Ning, R. Muller, T.-W. Yu, M. Taylor, D. Hoffman, C.-G. Kim, X. Zhang, C.R. Hutchinson, H.G. Floss, Biosynthesis of the ansamycin antibiotic rifamycin: deductions from the molecular analysis of the rif biosynthetic gene cluster of Amycolatopsis mediterranei S699, Chem. Biol. 5 (1998) 69-79.
44. R.M. Kagen, S. Clarke, Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes, Arch. Biochem. Biophys. 310 (1994) 417-427.
45. S.T. Cole, R. Brosch, J. Parkhill, T. Gamier, C. Churcher, D. Harris, S.V. Gordon, K. Eiglemeier, S. Gas, C.E. Barry, F. Tekaia III, K. Badcock, D. Basham, D. Brown, T. Chillingworth, R. Conner, R. Davies, K. Devlin, T. Feltwell, S. Gentles, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, A. Krogh, J. McLean, S. Moule, L. Murphy, K. Oliver, J. Osborne, M.A. Quail, M.-A. Rajandream, J. Rogers, S. Rutter, K. Seeger, J. Skelton, R. Squares, S. Squares, J.E. Sulston, K. Taylor, S. Whitehead, B.G. Barrell, Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence, Nature 393 (1998) 537-544.
46. B. Hube, F. Stehr, M. Bossenz, A. Mazur, M. Kretschmar, W. Schafer, Secreted lipases of Candida albicans: cloning, characterization and expression analysis of a new gene family with at least ten members, Arch. Microbiol. 174 (2000) 362-374.
47. J.D. Thompson, D.J. Higgins, T.J. Gibson, CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res. 22 (1994) 4673-4680.
48. R.H. Baltz, Gene expression in recombinant Streptomyces, Bioprocess. Technol. 22 (1995) 309-381.
49. M. Gilbert, R. Morosoli, F. Shareck, D. Kluepfel, Production and secretion of proteins by Streptomyces, Crit. Rev. Biotechnol. 15 (1995) 13-39.
50. J.L. Arpigny, K.E. Jaeger, Bacterial lipolytic enzymes: classification and properties, Biochem. J. 343 (1999) 177-183.
51. S. Kuhstoss, M. Huber, J.R. Turner, J.W. Paschal, R.N. Rao, Production of a novel polyketide through the construction of a hybrid polyketide synthase, Gene 183 (1996) 231-236.
52. A.R. Butler, N. Bate, E. Cundliffe, Impact of thioesterase activity on tylosin biosynthesis in Streptomyces fradiae, Chem. Biol. 6 (1999) 287-292.
53. S.G. Kendrew, K. Katayama, E. Deutch, K. Madduri, C.R. Hutchinson, DnrD cyclase involved in the biosynthesis of doxorubicin: purification and characterization of the recombinant enzyme, Biochemistry 38 (1999) 4794-4799.
54. R.H. Baltz, Mutagenesis in Streptomyces, in: A.L. Demain, N.A. Soloman (Eds.), Manual of Industrial Microbiology and Biotechnology, American Society for Microbiology, Washington, DC, 1986, pp. 184-190.
55. R.J. Strobel Jr., W.M. Nakatsukasa, Response surface methods for optimizing Saccharopolyspora spinosa, a novel macrolide producer, J. Ind. Microbiol. 11 (1993) 121-127.
56. L.C. Creemer, H.A. Kirst, J.W. Pashal, Conversion of spinosyn A and spinosyn D to their respective 9- and 17-pseudoaglycones and their aglycones, J. Antibiot. 51 (1998) 795-800.
57. D.A. Hopwood, M.J. Bibb, K.F. Chater, T. Kieser, C.J. Bruton, H.M. Kieser, D.J. Lydiate, C.P. Smith, J.M. Ward, H. Schrempf, Genetic Manipulation of Streptomyces: a Laboratory Manual, John Innes Foundation, Norwich, 1985.
58. T. Maniatis, E.F. Fritsch, J. Sambrook, Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Laboratory Press, Plainview, NY, 1982.
59. R. Simon, U. Preifer, A. Puhler, A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria, Bio/Technology 1 (1983) 784-791.
60. J.F. Aparacio, A.J. Colina, E. Ceballos, J.F. Martin, The biosynthetic cluster for the 26-membered ring polyene macrolide pimaricin, J. Biol. Chem. 274 (1999) 10133-10139.
61. V.T. Wilson, E. Cundliffe, Characterization and targeted disruption of a glycosyltransferase gene in the tylosin producer, Streptomyces fradiae, Gene 214 (1998) 95-100.
62. P.J. Solenberg, P. Matsushima, D.R. Stack, S.C. Wilkie, R.C. Thompson, R.H. Baltz, Production of hybrid glycopeptide antibiotics in vitro and in Streptomyces toyocaensis, Chem. Biol. 4 (1997) 195-202.