Identification and analysis of the chivosazol biosynthetic gene cluster from the myxobacterial model strain Sorangium cellulosum So ce56

Journal of Biotechnology

Volumn 121, Issue 2, 2006, Pages 174-191

  Perlova, Olena ^a   Gerth, Klaus ^b   Kaiser, Olaf ^c   Hans, Astrid ^b   Müller, Rolf ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c BIELEFELD UNIVERSITY   (Germany)

Author keywords

Biosynthetic gene cluster; Chivosazol; Myxobacteria; NRPS; PKS; Secondary metabolism; Sorangium cellulosum

Indexed keywords

ANTIBIOTICS; BACTERIA; BIOSYNTHESIS; CHROMOSOMES; ENZYMES; METABOLISM; YEAST;

BIOSYNTHETIC GENE CLUSTERS; CHIVOSAZOL; MYXOBACTERIA; NRPS; SECONDARY METABOLISM; SORANGIUM CELLULOSUM;

GENES;

ACTIN; ACYLTRANSFERASE; ANTIBIOTIC AGENT; CHIVOSAZOL; DEOXYGLUCOSE; MACROCYCLIC COMPOUND; METHYLTRANSFERASE; OXAZOLE; PEPTIDE SYNTHASE; POLYKETIDE SYNTHASE; QUINOVOSE; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CHROMOSOME; CONTROLLED STUDY; EUKARYOTIC CELL; GENE CLUSTER; GENE LOCUS; MYXOCOCCALES; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MODIFICATION; SORANGIUM CELLULOSUM;

GENES, BACTERIAL; LIGASES; MACROLIDES; MULTIENZYME COMPLEXES; MULTIGENE FAMILY; MYXOCOCCALES;

EUKARYOTA; FUNGI; MAMMALIA; MYXOCOCCALES; POLYANGIUM CELLULOSUM; SORANGIUM;

EID: 29844452482     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2005.10.011     Document Type: Article

References (71)

1. J.F. Aparicio, I. Molnar, T. Schwecke, A. Konig, S.F. Haydock, L.E. Khaw, J. Staunton, and P.F. Leadlay Organization of the biosynthetic gene cluster for rapamycin in Streptomyces hygroscopicus: analysis of the enzymatic domains in the modular polyketide synthase Gene 169 1996 9 16
2. V. Bergendahl, U. Linne, and M.A. Marahiel Mutational analysis of the C-domain in nonribosomal peptide synthesis Eur. J. Biochem. 269 2002 620 629
3. C. Bisang, P. Long, J. Cortes, J. Westcott, J. Crosby, A.-L. Matharu, R. Cox, T. Simpson, J. Staunton, and P. Leadlay A chain initiation factor common to both modular and aromatic polyketide synthases Nature 401 1999 502 505
4. D.M. Bollag, P.A. McQueney, J. Zhu, O. Hensens, L. Koupal, J. Liesch, M. Goetz, E. Lazarides, and M. Woods Epothilones, a new class of microtubule-stabilizing agents with taxol-like mechanism of action Cancer Res. 55 1995 2325 2333
5. P. Caffrey Conserved amino acid residues correlating with ketoreductase stereospecificity in modular polyketide synthases Chembiochem 4 2003 654 657
6. G.L. Challis, J. Ravel, and C.A. Townsend Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains Chem. Biol. 7 2000 211 224
7. Y.Q. Cheng, G.L. Tang, and B. Shen Identification and localization of the gene cluster encoding biosynthesis of the antitumor macrolactam leinamycin in Streptomyces atroolivaceus S-140 J. Bacteriol. 184 2002 7013 7024
8. Y.Q. Cheng, G.L. Tang, and B. Shen Type I polyketide synthase requiring a discrete acyltransferase for polyketide biosynthesis Proc. Natl. Acad. Sci. U.S.A. 100 2003 3149 3154
9. L. Du, M. Chen, C. Sanchez, and B. Shen An oxidation domain in the BlmIII non-ribosomal peptide synthetase probably catalyzing thiazole formation in the biosynthesis of the anti-tumor drug bleomycin in Streptomyces verticillus ATCC15003 FEMS Microbiol. Lett. 189 2000 171 175
10. A.K. El-Sayed, J. Hothersall, S.M. Cooper, E. Stephens, T.J. Simpson, and C.M. Thomas Characterization of the mupirocin biosynthesis gene cluster from Pseudomonas fluorescens NCIMB 10586 Chem. Biol. 10 2003 419 430
11. N. Gaitatzis, B. Silakowski, B. Kunze, G. Nordsiek, H. Blöcker, G. Höfle, and R. Müller The biosynthesis of the aromatic myxobacterial electron transport inhibitor stigmatellin is directed by a novel type of modular polyketide synthase J. Biol. Chem. 277 2002 13082 13090
12. N. Gaitatzis, B. Kunze, and R. Müller Novel insights into siderophore formation in myxobacteria Chembiochem 6 2005 365 374
13. K. Gerth, D. Schummer, G. Höfle, H. Irschik, and H. Reichenbach Ratjadon: a new antifungal compound from Sorangium cellulosum (myxobacteria) production, physio-chemical and biological properties J. Antibiot. (Tokyo) 48 1995 973 976
14. K. Gerth, N. Bedorf, G. Höfle, H. Irschik, and H. Reichenbach Epothilones A and B: antifungal and cytotoxic compounds from Sorangium cellulosum (Myxobacteria). Production, physico-chemical and biological properties J. Antibiot. (Tokyo) 49 1996 560 563
15. K. Gerth, S. Pradella, O. Perlova, S. Beyer, and R. Müller Myxobacteria: proficient producers of novel natural products with various biological activities-past and future biotechnological aspects with the focus on the genus Sorangium J. Biotechnol. 106 2003 233 253
16. M. He, M. Varoglu, and D.H. Sherman Structural modeling and site-directed mutagenesis of the actinorhodin beta-ketoacyl-acyl carrier protein synthase J. Bacteriol. 182 2000 2619 2623
17. T.M. Henkin Control of transcription termination in prokaryotes Annu. Rev. Genet. 30 1996 35 57
18. A.J. Herr, J.F. Atkins, and R.F. Gesteland Coupling of open reading frames by translational bypassing Annu. Rev. Biochem. 69 2000 343 372
19. G. Höfle, H. Steinmetz, K. Gerth, and H. Reichenbach Ambruticins VS: new members of the antifungal ambruticin family from Sorangium cellulosum Liebigs Ann. Chem. 1991 941 945
20. C.J. Ingham, I.S. Hunter, and M.C. Smith Rho-independent terminators without 3′ poly-U tails from the early region of actinophage øC31 Nucl. Acids Res. 23 1995 370 376
21. H. Irschik, R. Jansen, K. Gerth, G. Höfle, and H. Reichenbach The sorangicins, novel and powerful inhibitors of eubacterial RNA polymerase isolated from myxobacteria J. Antibiot. (Tokyo) 40 1987 7 13
22. H. Irschik, R. Jansen, K. Gerth, G. Höfle, and H. Reichenbach Chivosazol A, a new inhibitor of eukaryotic organisms isolated from myxobacteria J. Antibiot. (Tokyo) 48 1995 962 966
23. H. Irschik, R. Jansen, K. Gerth, G. Höfle, and H. Reichenbach Disorazol A, an efficient inhibitor of eukaryotic organisms isolated from myxobacteria J. Antibiot. (Tokyo) 48 1995 31 35
24. H. Irschik, R. Jansen, K. Gerth, G. Höfle, and H. Reichenbach Sorangiolid A, a new antibiotic isolated from the myxobacterium Sorangium cellulosum So ce 12 J. Antibiot. (Tokyo) 48 1995 886 887
25. R. Jansen, H. Irschik, H. Reichenbach, V. Wray, and G. Höfle Disorazoles, highly cytotoxic metabolites from the sorangicin-producing bacterium Sorangium cellulosum, strain So ce12 Liebigs Ann. Chem. 1994 759 773
26. R. Jansen, H. Irschik, H. Reichenbach, and G. Höfle Antibiotics from gliding bacteria, LXXX. Chivosazoles A-F: novel antifungal and cytotoxic macrolides from Sorangium cellulosum (Myxobacteria) Liebigs Ann. 1997 1725 1732
27. B. Julien, S. Shah, R. Ziermann, R. Goldman, L. Katz, and C. Khosla Isolation and characterization of the epothilone biosynthetic gene cluster from Sorangium cellulosum Gene 249 2000 153 160
28. B. Julien, and S. Shah Heterologous expression of epothilone biosynthetic genes in Myxococcus xanthus Antimicrob. Agents Chemother. 46 2002 2772 2778
29. O. Kaiser, D. Bartels, T. Bekel, A. Goesmann, S. Kespohl, A. Puhler, and F. Meyer Whole genome shotgun sequencing guided by bioinformatics pipelines - an optimized approach for an established technique J. Biotechnol. 106 2003 121 133
30. S.J. Kakavas, L. Katz, and D. Stassi Identification and characterization of the niddamycin polyketide synthase genes from Streptomyces caelestis J. Bacteriol. 179 1997 7515 7522
31. D. Konz, and M.A. Marahiel How do peptide synthetases generate structural diversity? Chem. Biol. 6 1999 R39 R48
32. M. Kopp, H. Irschik, F. Gross, O. Perlova, A. Sandmann, K. Gerth, and R. Müller Critical variations of conjugational DNA transfer into secondary metabolite multiproducing Sorangium cellulosum strains So ce12 and So ce56: development of a mariner-based transposon mutagenesis system J. Biotechnol. 107 2004 29 40
33. M. Kopp, H. Irschik, S. Pradella, and R. Müller Production of the tubulin destabilizer disorazol in Sorangium cellulosum: biosynthetic machinery and regulatory genes Chembiochem 6 2005 1277 1286
34. H.-J. Kwon, W.C. Smith, A.J. Scharon, S.H. Hwang, M.J. Kurth, and B. Shen C-O bond formation by polyketide synthases Science 297 2002 1327 1330
35. M.R. Langer, C.J. Fry, C.L. Peterson, and J.M. Denu Modulating acetyl-CoA binding in the GCN5 family of histone acetyltransferases J. Biol. Chem. 277 2002 27337 27344
36. J. Ligon, S. Hill, J. Beck, R. Zirkle, I. Monar, J. Zawodny, S. Money, and T. Schupp Characterization of the biosynthetic gene cluster for the antifungal polyketide soraphen A from Sorangium cellulosum So ce26 Gene 285 2002 257 267
37. P.F. Long, C.J. Wilkinson, C.P. Bisang, J. Cortes, N. Dunster, M. Oliynyk, E. McCormick, H. McArthur, C. Mendez, J.A. Salas, J. Staunton, and P.F. Leadlay Engineering specificity of starter unit selection by the erythromycin-producing polyketide synthase Mol. Microbiol. 43 2002 1215 1225
38. C.G. Marshall, N.J. Hillson, and C.T. Walsh Catalytic mapping of the vibriobactin biosynthetic enzyme VibF Biochemistry 41 2002 244 250
39. S. Mochizuki, K. Hiratsu, M. Suwa, T. Ishii, F. Sugino, K. Yamada, and H. Kinashi The large linear plasmid pSLA2-L of Streptomyces rochei has an unusually condensed gene organization for secondary metabolism Mol. Microbiol. 48 2003 1501 1510
40. I. Molnar, T. Schupp, M. Ono, R. Zirkle, M. Milnamow, B. Nowak-Thompson, N. Engel, C. Toupet, A. Stratmann, D.D. Cyr, J. Gorlach, J.M. Mayo, A. Hu, S. Goff, J. Schmid, and 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
41. H.D. Mootz, D. Schwarzer, and M.A. Marahiel Ways of assembling complex natural products on modular nonribosomal peptide synthetases Chembiochem 3 2002 490 504
42. S.J. Moss, C.J. Martin, and B. Wilkinson Loss of co-linearity by modular polyketide synthases: a mechanism for the evolution of chemical diversity Nat. Prod. Rep. 21 2004 575 593
43. R. Müller Don't classify polyketide synthases Chem. Biol. 11 2004 4 6
44. C. Olano, B. Wilkinson, C. Sanchez, S.J. Moss, R. Sheridan, V. Math, A.J. Weston, A.F. Brana, C.J. Martin, M. Oliynyk, C. Mendez, P.F. Leadlay, and J.A. Salas Biosynthesis of the angiogenesis inhibitor borrelidin by Streptomyces parvulus Tu4055: cluster analysis and assignment of functions Chem. Biol. 11 2004 87 97
45. A. Pereda, R.G. Summers, D.L. Stassi, X. Ruan, and L. Katz The loading domain of the erythromycin polyketide synthase is not essential for erythromycin biosynthesis in Saccharopolyspora erythraea Microbiology 144 Pt 2 1998 543 553
46. J. Piel A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles Proc. Natl. Acad. Sci. U.S.A. 99 2002 14002 14007
47. S. Pradella, A. Hans, C. Sproer, H. Reichenbach, K. Gerth, and S. Beyer Characterisation, genome size and genetic manipulation of the myxobacterium Sorangium cellulosum So ce56 Arch. Microbiol. 178 2002 484 492
48. H. Reichenbach, and G. Höfle Biologically active secondary metabolites from myxobacteria Biotechnol. Adv. 11 1993 219 277
49. R. Reid, M. Piagentini, E. Rodriguez, G. Ashley, N. Viswanathan, J. Carney, D.V. Santi, C.R. Hutchinson, and R. McDaniel A model of structure and catalysis for ketoreductase domains in modular polyketide synthases Biochemistry 42 2003 72 79
50. J. Sambrook E.F. Fritsch T. Maniatis Molecular Cloning: A Laboratory Manual 1989 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
51. A. Sandmann, F. Sasse, and R. Müller Identification and analysis of the core biosynthetic machinery of tubulysin, a potent cytotoxin with potential anticancer activity Chem. Biol. 11 2004 1071 1079
52. T.L. Schneider, B. Shen, and C.T. Walsh Oxidase domains in epothilone and bleomycin biosynthesis: thiazoline to thiazole oxidation during chain elongation Biochemistry 42 2003 9722 9730
53. N.S. Scrutton, A. Berry, and R.N. Perham Redisign of the coenzyme specificity of a dehydrogenase by protein engineering Nature 343 1990 38 43
54. B. Shen Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms Curr. Opin. Chem. Biol. 7 2003 285 295
55. B. Silakowski, H.U. Schairer, H. Ehret, B. Kunze, S. Weinig, G. Nordsiek, P. Brandt, H. Blöcker, G. Höfle, S. Beyer, and R. Müller New lessons for combinatorial biosynthesis from myxobacteria: the myxothiazol biosynthetic gene cluster of Stigmatella aurantiaca DW4/3-1 J. Biol. Chem. 274 1999 37391 37399
56. B. Silakowski, G. Nordsiek, B. Kunze, H. Blöcker, and R. Müller Novel features in a combined polyketide synthase/non-ribosomal peptide synthetase: the myxalamid biosynthetic gene cluster of the myxobacterium Stigmatella aurantiaca Sga15 Chem. Biol. 8 2001 59 69
57. R. Simon, M. O'Connell, M. Labes, and A. Pühler Plasmid vectors for the genetic analysis and manipulation of rhizobia and other gram-negative bacteria Meth. Enzymol. 118 1986 643 659
58. T. Stachelhaus, H.D. Mootz, and M.A. Marahiel The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases Chem. Biol. 6 1999 493 505
59. J. Staunton, and K.J. Weissman Polyketide biosynthesis: a millennium review Nat. Prod. Rep. 18 2001 380 416
60. G.L. Tang, Y.Q. Cheng, and B. Shen Leinamycin biosynthesis revealing unprecedented architectural complexity for a hybrid polyketide synthase and nonribosomal peptide synthetase Chem. Biol. 11 2004 33 45
61. L. Tang, S. Ward, L. Chung, J.R. Carney, Y. Li, R. Reid, and L. Katz Elucidating the mechanism of cis double bond formation in epothilone biosynthesis J. Am. Chem. Soc. 126 2004 46 47
62. C.T. Walsh, A.M. Gehring, P.H. Weinreb, L.E. Quadri, and R.S. Flugel Post-translational modification of polyketide and nonribosomal peptide synthases Curr. Opin. Chem. Biol. 1 1997 309 315
63. C.T. Walsh, H.W. Chen, T.A. Keating, B.K. Hubbard, H.C. Losey, L.S. Luo, C.G. Marshall, D.A. Miller, and H.M. Patel Tailoring enzymes that modify nonribosomal peptides during and after chain elongation on NRPS assembly lines Curr. Opin. Chem. Biol. 5 2001 525 534
64. C.T. Walsh Polyketide and nonribosomal peptide antibiotics: modularity and versatility Science 303 2004 1805 1810
65. S. Weinig, H.J. Hecht, T. Mahmud, and R. Müller Melithiazol biosynthesis: further insights into myxobacterial PKS/NRPS systems and evidence for a new subclass of methyl transferases Chem. Biol. 10 2003 939 952
66. K.J. Weissman, M. Bycroft, J. Staunton, and P.F. Leadlay Origin of starter units for erythromycin biosynthesis Biochemistry 37 1998 11012 11017
67. S.C. Wenzel, F. Gross, Y. Zhang, J. Fu, A.F. Stewart, and R. Müller Heterologous expression of a myxobacterial natural products assembly line in pseudomonads via Red/ET recombineering Chem. Biol. 12 2005 349 356
68. S.C. Wenzel, and R. Müller Formation of novel secondary metabolites by bacterial multimodular assembly lines: deviations from text book biosynthetic logic Curr. Opin. Chem. Biol. 9 2005 447 458
69. Y. Xue, L. Zhao, H.W. Liu, and D.H. Sherman A gene cluster for macrolide antibiotic biosynthesis in Streptomyces venezuelae: architecture of metabolic diversity Proc. Nat. Acad. Sci. U.S.A. 95 1998 12111 12116
70. G. Yadav, R.S. Gokhale, and D. Mohanty Computational approach for prediction of domain organization and substrate specificity of modular polyketide synthases J. Mol. Biol. 328 2003 335 363
71. R. Zirkle, J.M. Ligon, and I. Molnar Heterologous production of the antifungal polyketide antibiotic soraphen A of Sorangium cellulosum So ce26 in Streptomyces lividans Microbiology 150 2004 2761 2774