A study of iterative type II polyketide synthases, using bacterial genes cloned from soil DNA: A means to access and use genes from uncultured microorganisms

Journal of Bacteriology

Volumn 179, Issue 23, 1997, Pages 7360-7368

  Seow, Kah Tong ^a,d   Meurer, Guido ^b   Gerlitz, Martin ^b   Wendt Pienkowski, Evelyn ^b   Hutchinson, C Richard ^b   Davies, Julian ^a,c  

^a Terragen Diversity Inc   (Canada)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; POLYKETIDE; SYNTHETASE;

ARTICLE; BACTERIAL GENE; BACTERIUM MUTANT; BIOSYNTHESIS; GENOME; MOLECULAR CLONING; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SOIL MICROFLORA; STREPTOMYCES;

EID: 0030690924     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.23.7360-7368.1997     Document Type: Article

References (74)

1. Arrowsmith, T. J., F. Malpartida, D. H. Sherman, A. Birch, D. A. Hopwood, and J. A. Robinson. 1992. Characterization of actI-homologous DNA encoding polyketide synthase genes from the monensin producer Streptomyces cinnamonensis. Mol. Gen. Genet. 234:254-264.
2. Atlas, R. M. 1982. Enumeration and estimation of microbial biomass, p. 84-102. In R. G. Burns and J. H. Slater (ed.), Experimental microbial ecology. Blackwell Scientific Publications Ltd., Oxford, England.
3. Beck, J., S. Ripka, A. Siegner, E. Schiltz, and E. Schweizer. 1990. The multifunctional 6-methylsalicylic acid synthase gene of Penicillium patulum: its gene structure relative to that of other polyketide synthases. Eur. J. Biochem. 192:487-498.
4. Bergh, S., and M. Uhlén. 1992. Analysis of a polyketide synthesis-encoding gene cluster of Streptomyces curacoi. Gene 117:131-136.
5. Bibb, M. J., S. Biro, H. Motamedi, J. F. Collins, and C. R. Hutchinson. 1989. Analysis of the nucleotide sequence of the Streptomyces glaucescens tcmI genes provides key information about the enzymology of polyketide tetracenomycin C antibiotic biosynthesis. EMBO J. 8:2727-2736.
6. Bibb, M. J., D. H. Sherman, S. Omura, and D. A. Hopwood. 1994. Cloning, sequencing and deduced functions of a cluster of Streptomyces genes probably encoding biosynthesis of the polyketide antibiotic frenolicin. Gene 142:31-39.
7. Blanco, G., A. Pereda, P. Brian, C. Mendez, K. F. Chater, and J. A. Salas. 1993. A hydroxylase-like gene product contributes to synthesis of a polyketide spore pigment in Streptomyces halstedii. J. Bacteriol. 175:8043-8048.
8. Bormann, C., K. Aberle, H.-P. Fiedler, and H. Schrempf. 1990. Genetic complementation of Streptomyces tendae deficient in nikkomycin production. Appl. Microbiol. Biotechnol. 32:424-430.
9. Brown, D. W., J. H. Yu, H. S. Kelkar, M. Fernandas, R. C. Nesbitt, N. P. Keller, T. H. Adams, and T. J. Leonard. 1996. Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA 93:1418-1422.
10. Byrne, K. M., B. D. Hilton, R. J. White, R. Misra, and R. C. Pandey. 1985. Biosynthesis of fredericamycin A, a new antitumor antibiotic. Biochemistry 24:478-486.
11. Cortes, J., S. F. Haydock, G. A. Roberts, D. J. Bevitt, and P. F. Leadlay. 1990. An unusually large multifunctional polypeptide in the erythromycin-producing polyketide synthase of Saccharopolyspora erythraea. Nature 348:176-178.
12. Cortes, J., K. E. H. Wiesmann, G. A. Roberts, M. J. B. Brown, J. Staunton, and P. F. Leadlay. 1995. Repositioning of a domain in a modular polyketide synthase to promote specific chain cleavage. Science 268:1487-1489.
13. Davis, N. K., and K. F. Chater. 1990. Spore colour in Streptomyces coelicolor A3(2) involves the developmentally regulated synthesis of a compound biosynthetically related to polyketide antibiotics. Mol. Microbiol. 4:1679-1691.
14. Decker, H., H. Motamedi, and C. R. Hutchinson. 1993. The nucleotide sequence and heterologous expression of tcmG and tcmP, biosynthetic genes for tetracenomycin C in Streptomyces glaucescens. J. Bacteriol. 175:3876-3886.
15. Decker, H., and S. Haag. 1995. Cloning and characterization of a polyketide synthase gene from Streptomyces fradiae Tü2717, which carries the genes for biosynthesis of the angucycline antibiotic urdamycin A and a gene probably involved in its oxygenation. J. Bacteriol. 177:6126-6136.
16. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
17. Donadio, S., M. J. Staver, J. B. McAlpine, S. J. Swanson, and L. Katz. 1991. Modular organization of genes required for complex polyketide biosynthesis. Science 759:675-679.
18. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
19. Fernandez-Moreno, M. A., E. Martinez, L. Boto, D. A. Hopwood, and F. Malpartida. 1992. Nucleotide sequence and deduced functions of a set of co-transcribed genes of Streptomyces coelicolor A3(2) including the polyketide synthase for the antibiotic actinorhodin. J. Biol. Chem. 267:19278-19290.
20. Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J. F. Tomb, B. A. Dougherty, and J. M. Merrick. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae. Science 269:496-512.
21. Fu, H., D. A. Hopwood, and C. Khosla. 1995. Engineered biosynthesis of novel polyketides: evidence for temporal, but not regiospecific, control of cyclization of an aromatic polyketide precursor. Chem. Biol. 1:205-210.
22. Galmarini, O. L., and V. Deulofeu. 1961. Curamycin. I. Isolation and characterization of some hydrolysis products. Tetrahedron 15:76-86.
23. Grimm, A., K. Madduri, A. Ali, and C. R. Hutchinson. 1994. Characterization of the Streptomyces peucetius ATCC 29050 genes encoding doxorubcin polyketide synthase. Gene 151:1-10.
24. Han, L., K. Yang, E. Ramalingam, R. H. Mosher, and L. C. Vining. 1994. Cloning and characterization of polketide synthase genes for jadomycin B biosynthesis in Streptomyces venezuelae. Microbiology 140:3379-3389.
25. Holben, W. E., J. K. Jansson, B. K. Chelm, and J. M. Tiedje. 1988. DNA probe method for the detection of specific microorganisms in the soil bacterial community. Appl. Environ. Microbiol. 54:703-711.
26. Hopwood, D. A., T. Kieser, H. M. Wright, and M. J. Bibb. 1983. Plasmids, recombination and chromosome mapping in Streptomyces lividans 66. J. Gen. Microbiol. 129:2257-2269.
27. Hopwood, D. A., M. J. Bibb, K. F. Chater, T. Kieser, C. J. Bruton, H. M. Kieser, D. J. Lydiate, C. P. Smith, J. M. Ward, and H. Schrempf. 1985. Genetic manipulation of Streptomyces. A laboratory manual. The John Innes Foundation, Norwich, United Kingdom.
28. Hutchinson, C. R. 1997. Antibiotics from genetically engineered microorganisms, p. 659-682. In W. R. Strohl (ed.), Biotechnology of industrial antibiotics. Marcel Dekker, Baltimore, Md.
29. Hutchinson, C. R., and I. Fujii. 1995. Polyketide synthase gene manipulation: a structure-function approach in engineering novel antibiotics. Annu. Rev. Microbiol. 49:201-238.
30. Jensen, P. R., and W. Fenical. 1994. Strategies for the discovery of secondary metabolites from marine bacteria: ecological perspectives. Annu. Rev. Microbiol. 48:559-584.
31. Kao, C. M., G. Luo, L. Katz, D. E. Cane, and C. Khosla. 1994. Engineered biosynthesis of a triketide lactone from an incomplete modular polyketide synthase. J. Am. Chem. Soc. 116:11612-11613.
32. Kao, C. M., G. Luo, L. Katz, D. E. Cane, and C. Khosla. 1995. Manipulation of macrolide ring size by directed mutagenesis of a modular polyketide synthase. J. Am. Chem. Soc. 117:9105-9106.
33. Katz, L., and S. Donadio. 1993. Polyketide synthesis: Prospects for hybrid antibiotics. Annu. Rev. Microbiol. 47:875-912.
34. Kauppinen, S., M. Siggaard-Andersen, and P. von-Wettstein-Knowles. 1988. β-Ketoacyl-ACP synthase I of Escherichia coli: nucleotide sequence of the fabB gene and identification of the cerulenin binding residue. Carlsberg Res. Commun. 53:357-370.
35. Khosla, C. Personal communication.
36. Kim, E. S., M. J. Bibb, M. J. Butler, D. A. Hopwood, and D. H. Sherman. 1994. Sequences of the oxytetracycline polyketide synthase-encoding otc genes from Streptomyces rimosus. Gene 141:141-142.
37. Kim, E. S., K. D. Cramer, A. L. Shreve, and D. H. Sherman. 1995. Heterologous expression of an engineered biosynthetic pathway: functional dissection of type II polyketide synthase components in Streptomyces species. J. Bacteriol. 177:1202-1207.
38. Kramer, P. J., R. J. X. Zwada, R. McDaniel, C. R. Hutchinson, D. A. Hopwood, and C. Khosla. 1997. Rational design and engineered biosynthesis of a novel 18-carbon aromatic polyketide. J. Am. Chem. Soc. 119:635-639.
39. Le, G. C., D. Desmarais, and C. V. Dery. 1993. Saccharopolyspora hirsuta 367 encodes clustered polyketide synthases, polyketide reductase, acyl carrier protein, and biotin carboxyl carrier protein homologous genes. Mol. Gen. Genet. 240:146-150.
40. Lombo, F., G. Blanco, E. Fernandez, C. Mendez, and J. A. Salas. 1996. Characterization of Streptomyces argillaceus genes encoding a polyketide synthase involved in the biosynthesis of the antitumor antibiotic mithramycin. Gene 172:87-91.
41. MacNeil, D. J., J. L. Occi, K. M. Gewain, and T. MacNeil. 1994. Correlation of the avermectin polyketide synthase genes to the avermectin structure: implications for designing novel avermectins. Ann. N.Y. Acad. Sci. 721:123-132.
42. McDaniel, R., S. Ebert-Khosla, D. A. Hopwood, and C. Khosla. 1993. Engineered biosynthesis of novel polyketides. Science 262:1546-1550.
43. McDaniel, R., S. Ebert-Khosla, D. A. Hopwood, and C. Khosla. 1994. Engineered biosynthesis of novel polyketides: actVII and actIV genes encode aromatase and cyclase enzymes, respectively. J. Am. Chem. Soc. 116:10855-10859.
44. McDaniel, R., S. Ebert-Khosla, H. Fu, D. A. Hopwood, and C. Khosla. 1994. Engineered biosynthesis of novel polyketides: influence of a downstream enzyme on the catalytic specificity of a minimal aromatic polyketide synthase. Proc. Natl. Acad. Sci. USA 91:11542-11546.
45. McDaniel, R., S. Ebert-Khosla, D. A. Hopwood, and C. Khosla. 1995. Rational design of aromatic polyketide natural products by recombinant assembly of enzymatic subunits. Nature 375:549-554.
46. McDaniel, R., C. R. Hutchinson, and C. Khosla. 1995. Engineered biosynthesis of novel polyketides: analysis of tcmN function in tetracenomycin biosynthesis. J. Am. Chem. Soc. 117:6805-6810.
47. Meurer, G., and C. R. Hutchinson. 1995. Functional analysis of putative β-ketoacyl:acyl carrier protein synthase and acyltransferase active-site motifs in a type II polyketide synthase of Streptomyces glaucescens. J. Bacteriol. 177:477-481.
48. Monaghan, R. L., and J. S. Tkacz. 1990. Bioactive microbial products: focus on mechanism of action. Annu. Rev. Microbiol. 44:271-301.
49. Morris, N. Z., H. Gürtler, P. Revill, and E. M. H. Wellington. 1997. Distribution and diversity of type II polyketide synthase genes in soil populations of actinomycetes colonising crops in Cuban soils, abstr. 1P19. In Abstracts of the 10th International Symposium on Biology of Actinomycetes.
50. Motamedi, H., E. Wendt-Pienkowski, and C. R. Hutchinson. 1986. Isolation of tetracenomycin C-nonproducing Streptomyces glaucescens mutants. J. Bacteriol. 167:575-580.
51. Motamedi, H., and C. R. Hutchinson. 1987. Cloning and heterologous expression of a gene cluster for the biosynthesis of tetracenomycin C, the anthracycline antitumor antibiotic of Streptomyces glaucescens. Proc. Natl. Acad. Sci. USA 84:4445-4449.
52. O'Hagan, D. 1991. The polyketide metabolites. Horwood, Chichester, United Kingdom.
53. Piecq, M., P. Dehottay, A. Biot, and J. Dusart. 1994. Cloning and nucleotide sequence of a region of the Kibdelosporangium aridum genome homologous to polyketide biosynthetic genes. DNA Sequence 4:219-229.
54. Rajgarhia, V. B., and W. R. Strohl. 1997. Minimal Streptomyces sp. strain C5 daunorubicin polyketide biosynthesis genes required for aklanonic acid biosynthesis. J. Bacteriol. 179:2690-2696.
55. Saiton, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
56. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
57. Schupp, T., C. Toupet, B. Cluzel, S. Neff, S. Hill, J. J. Beck, and J. Ligon. 1995. A Sorangium cellulosum (Myxobacterium) gene cluster for the biosynthesis of the macrolide antibiotic soraphen A: cloning, characterization, and homology to polyketide synthase genes from actinomycetes. J. Bacteriol. 177:3673-3679.
58. Schwecke, T., J. F. Aparicio, I. Molnar, A. Konig, L. E. Khaw, S. F. Haydock, M. Oliynyk, P. Caffrey, J. Cortes, J. B. Lester, G. A. Bohm, J. Staunton, and P. F. Leadlay. 1995. The biosynthesis gene cluster for the polyketide immunosuppressant rapamycin. Proc. Natl. Acad. Sci. USA 92:7839-7843.
59. Seow, K. T., and J. E. Davies. Unpublished data.
60. Shen, B., R. G. Summers, E. Wendt-Pienkowski, and C. R. Hutchinson. 1995. The Streptomyces glaucescens tcmKL polyketide synthase gene and tcmN polyketide cyclase genes govern the size and shape of aromatic polyketides. J. Am. Chem. Soc. 117:6811-6821.
61. Shen, B., and C. R. Hutchinson. 1996. Deciphering the mechanism for the assembly of aromatic polyketides by a bacterial polyketide synthase. Proc. Natl. Acad. Sci. USA 93:6600-6604.
62. Sherman, D. H., F. Malpartida, M. J. Bibb, H. M. Kieser, M. J. Bibb, and D. A. Hopwood. 1989. Structure and deduced function of the granaticin-producing polyketide synthase gene cluster of Streptomyces violaceoruber TU22. EMBO J. 8:2717-2725.
63. Sherman, D. H., E.-S. Kim, M. J. Bibb, and D. A. Hopwood. 1992. Functional replacement of genes for individual polyketide synthase components in Streptomyces coelicolor A3(2) by heterologous genes from a different polyketide pathway. J. Bacteriol. 174:6184-6190.
64. Shizuya, H., B. Birren, U.-J. Kim, V. Mancino, T. Slepak, Y. Tachiiri, and M. Simon. 1992. Cloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Proc. Natl. Acad. Sci. USA 89:8794-8797.
65. Stachelhaus, T., A. Schneider, and M. A. Marahiel. 1995. Rational design of peptide antibiotics by targeted replacement of bacterial and fungal domains. Science 269:69-72.
66. Stachelhaus, T., A. Schneider, and M. A. Marahiel. 1996. Engineered biosynthesis of peptide antibiotics. Biochem. Pharmacol. 52:177-186.
67. Summers, R. G., E. Wendt-Pienkowski, H. Motamedi, and C. R. Hutchinson. 1992. Nucleotide sequence of the tcmNO region of the tetracenomycin C biosynthetic gene cluster of Streptomyces glaucescens and evidence that the tcmN gene encodes a multifunctional cyclase/dehydratase/O-methyltransferase. J. Bacteriol. 174:1810-1820.
68. Summers, R. G., E. Wendt-Pienkowski, H. Motamedi, and C. R. Hutchinson. 1993. The tcmVI region of the tetracenomycin C biosynthetic gene cluster of Streptomyces glaucescens encodes the tetracenomycin F1 monooxygenase, tetracenomycin F2 cyclase, and, most likely, a second cyclase. J. Bacteriol. 175:7571-7580.
69. Torsvik, V., J. Goksøyr, and F. L. Daae. 1990. High diversity in DNA of soil bacteria. Appl. Environ. Microbiol. 56:782-787.
70. Vara, J., M. Lewandowska-Skarbek, Y.-G. Wang, S. Donadio, and C. R. Hutchinson. 1989. Cloning of genes governing the deoxysugar portion of the erythromycin biosynthetic pathway in Saccharopolyspora erythraea (Streptomyces erythreus). J. Bacteriol. 171:5872-5881.
71. Ye, J., M. L. Dickens, R. Plater, Y. Li, J. Lawrence, and W. R. Strohl. 1994. Isolation and sequence analysis of polyketide synthase genes from the daunomycin-producing Streptomyces sp. strain C5. J. Bacteriol. 176:6270-6280.
72. Ylihonko, K., J. Tuikkanen, S. Jussila, L. Cong, and P. Mantsala. 1996. A gene cluster involved in nogalamycin biosynthesis from Streptomyces nogalater: sequence analysis and complementation of early-block mutations in the anthracycline pathway. Mol. Gen. Genet. 251:113-120.
73. Yu, T. W., M. J. Bibb, W. P. Revill, and D. A. Hopwood. 1994. Cloning, sequencing, and analysis of the griseusin polyketide synthase gene cluster from Streptomyces griseus. J. Bacteriol. 176:2627-2634.
74. Zawada, R. J. X., and C. Khosla. 1997. Domain analysis of the molecular recognition features of aromatic polyketide synthase subunits. J. Biol. Chem. 272:16184-16188.