Insights into the evolution of macrolactam biosynthesis through cloning and comparative analysis of the biosynthetic gene cluster for a novel macrocyclic lactam, ML-449

Applied and Environmental Microbiology

Volumn 76, Issue 1, 2010, Pages 283-293

  Jørgensen, Hanne ^a   Degnes, Kristin F ^b   Dikiy, Alexander ^a   Fjærvik, Espen ^a   Klinkenberg, Geir ^b   Zotchev, Sergey B ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b SINTEF MATERIALS AND CHEMISTRY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHETIC GENE CLUSTER; BIOSYNTHETIC PATHWAY; CLONING AND SEQUENCING; COMPARATIVE ANALYSIS; EVOLUTIONARY RELATIONSHIPS; GENE CLUSTERS; KETOSYNTHASE; MACROCYCLICS; MACROLACTONES; MARINE SEDIMENTS; PHYLOGENETIC ANALYSIS; POLYENE MACROLIDE; POLYKETIDE SYNTHASES; SIDE CHAINS; STREPTOMYCES SP;

BIOCHEMISTRY; CLONING; ORGANIC COMPOUNDS; SEDIMENTS; SUBMARINE GEOLOGY;

BIOSYNTHESIS;

BACTERIAL DNA; BACTERIAL PROTEIN; MACROCYCLIC LACTAM; POLYKETIDE SYNTHASE;

ANTIBIOTICS; BACTERIUM; BIOTECHNOLOGY; COMPARATIVE STUDY; GENE; MARINE SEDIMENT; MARINE TECHNOLOGY; PHYLOGENETICS;

ARTICLE; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; CLUSTER ANALYSIS; DNA SEQUENCE; GENE ORDER; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEDIMENT; SEQUENCE HOMOLOGY; STREPTOMYCES;

BACTERIAL PROTEINS; BIOSYNTHETIC PATHWAYS; CLONING, MOLECULAR; CLUSTER ANALYSIS; DNA, BACTERIAL; EVOLUTION, MOLECULAR; GENE ORDER; GEOLOGIC SEDIMENTS; LACTAMS, MACROCYCLIC; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MULTIGENE FAMILY; PHYLOGENY; POLYKETIDE SYNTHASES; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; STREPTOMYCES;

STREPTOMYCES SP.;

EID: 76149089531     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00744-09     Document Type: Article

References (45)

1. Anisimova, M., and O. Gascuel. 2006. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 55:539-552.
2. Bisang,C.,P.F.Long,J.Cortés,J.Westcott,J.Crosby,A.-L.Matharu,R.J. Cox,T.J.Simpson,J.Stauntonk,andP.F.Leadlay.1999.Achaininitiationfactorcommon- bothmodularandaromaticpolyketidesynthases.Nature401:502-505.(Pubitemid129515791)
3. Bredholt,H.,E.Fjærvik,G.Johnsen,andS.B.Zotchev.2008. ActinomycetesfromsedimentsintheTrondheimfjord,Norway: diversityandbiologicalactivity.Mar.Drugs6:12-24.(Pubitemid351543687)
4. Bruheim, P., S. E. F. Borgos, P. Tsan, H. Sletta, T. E. Ellingsen, J.-M. Lancelin, and S. B. Zotchev. 2004. Chemical diversity of polyene macrolides produced by Streplomyces noursei ATCC 1.1455 and recombinant strain ERD44 with genetically altered polyketide synthase NysC. Antimicrob. Agents Chemother. 48:4120-4129.
5. Carver, T. J., K. M. Rutherford, M. Berriman, M. A. Rajandream, B. G. Barrell, and J. Parkhlll. 2005. ACT: the Artemis Comparison Tool. Bioinformatics 21:3422-3423.
6. Cheng, Y.-Q., G.-L. Tang, and B. Shen. 2003. Type I polyketide synthase requiring a discrete acyltransferase for polyketide biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 100:3149-3154.
7. Duitman, E. H., L. W. Hamoen, M. Rembold, G. Venema, H. Seitz, W. Saenger, F. Bernhard, R. Reinhardt, M. Schmidt, C. Ullrich, T. Stein, F. Leenders, and J. Vater. 1999. The mycosubtilin synthetase of Bacillus subtilis ATCC6633: a multifunctional hybrid between a peptide synthetase, an amino transferase, and a fatty acid synthase. Proc. Natl. Acad. Sci. U. S. A. 96:13294-13299.
8. Fewer, D. P., L. Rouhiainen, J. Jokela, M. Wahlsten, K. Laakso, H. Wang, and K. Sivonen. 2007. Recurrent adenylation domain replacement in the microcystin synthetase gene cluster. BMC Evol. Biol. 7:183.
9. Fischbach, M. A., and C. T. Walsh. 2006. Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms. Chem. Rev. 106:3468-3496.
10. Flett, F., V. Mersinias, and C. P. Smith. 1997. High efficiency intergeneric conjugal transfer of plasmid DNA from Escherichia coli to methyl DNA-restricting streptomycetes. FEMS Microbiol. Lett. 155:223-229.
11. Ginolhac, A., C. Jarrin, P. Robe, G. Perrière, T. M. Vogel, P. Simonet, and R. Nalin. 2005. Type I polyketide synthases may have evolved through horizontal gene transfer. J. Mol. Evol. 60:716-725.
12. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
13. Hall, B. G. 2008. Phylogenetic trees made easy: a how-to manual, 3rd ed. Sinauer Associates, Inc., Sunderland, MA.
14. Ishikawa, J., and K. Hotta. 1999. FramePlot: a new implementation of the frame analysis for predicting protein-coding regions in bacterial DNA with a high G+C content. FEMS Microbiol. Lett. 174:251-253.
15. Izumikawa, M., M. Murata, K. Tachibana, Y. Ebizukac, and I. Fujii. 2003. Cloning of modular type I polyketide synthase genes from salinomycin producing strain of Streplomyces albus. Bioorg. Med. Chem. 11:3401-3405.
16. Jenke-Kodama, H., A. Sandmann, R. Millier, and E. Dittmann. 2005. Evolutionary implications of bacterial polyketide synthases. Mol. Biol. Evol. 22:2027-2039.
17. Jenke-Kodama, H., T. Borner, and E. Dittmann. 2006. Natural biocombinatorics in the polyketide synthase genes of the actinobacterium Streptomyces avermitilis. PLoS Comput. Biol. 2:e132.
18. Jørgensen, H., E. Fjærvik, S. Hakvåg, P. Bruheim, H. Bredholt, G. Klinkenberg, T. E. Ellingsen, and S. B. Zotchev. 2009. Candicidin biosynthetic gene cluster is widely distributed among Streptomyces spp. isolated from the sediments and the neusten layer of the Trondheims fjord, Norway. Appl. Environ. Microbiol. 75:3296-3303.
19. Jørgensen, H., K. F. Degnes, H. Sletta, E. Fjærvik, A. Dikiy, L. Herfindal, P. Bruheim, G. Klinkenberg, H. Bredholt, S. O. Daskeland, and S. B. Zotchev. 2009. Biosynthesis of macrolactam BE-14106 involves two distinct PKS systems and amino acid processing enzymes for generation of the aminoacyl starter unit. Chem. Biol. 16:1109-1121.
20. Keating, T. A., Z. Suo, D. E. Ehmann, and C. T. Walsh. 2000. Selectivity of the yersmiabactin synthetase adenylation domain in the two-step process of amino acid activation and transfer to a holo-carrier protein domain. Biochemistry 39:2297-2306.
21. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streplomyces genetics. The John Innes Foundation, Norwich, United Kingdom.
22. Kojiri, K., S. Nakajima, H. Suzuki, H. Kondo, and H. Suda. 1992. A new macrocydic lactam antibiotic, BE-14106. I. Taxonomy, isolation, biological activity and structural elucidation. J. Antibiot. (Tokyo) 45:868-874.
23. Kopp, M., H. Irschik, S. Pradella, and R. Müller. 2005. Production of the tubulin destabilizer disorazol in Sorangium cellulosum: biosynthetic machinery and regulatory genes. Chembiochem 6:1277-1286.
24. Long, P. F., C. J. Wilkinson, C. P. Bisang, J. Cortés, N. Dunster, M. Oliynyk, E. McCormick, H. McArthur, C. Mendez, J. A. Salas, J. Staunton, and P. F. Leadlay. 2002. Engineering specificity of starter unit selection by the eryth-romycin-producing polyketide synthase. Mol. Microbiol, 43:1215-1225.
25. Lopez, J. V. 2003. Naturally mosaic operons for secondary metabolite biosynthesis: variability and putative horizontal transfer of discrete catalytic domains of the epothilone polyketide synthase locus. Mol. Genet. Genomics 270:420-431.
26. Marahiel, M. A., T. Stachclhaus, and H. D. Mootz. 1997. Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 97: 2651-2674.
27. Menzella, H. G., and C. D. Reeves. 2007. Combinatorial biosynthesis for drug development. Curr. Opin. Microbiol. 10:238-245.
28. Muffitt, M. C., and B. A. Neilan. 2003. Evolutionary affiliations within the superfamily of ketosynthases reflect complex pathway associations. J. Mol. Evol. 56:446-457.
29. Nguyen, T., K. Ishida, H. Jenke-Kodama, E. Dittmann, C. Gurgui, T. Hochmuth, S. Taudien, M. Platzer, C. Hertweck, and J. Piel. 2008. Exploiting the mosaic structure of trans-acyltransferase polyketide synthases for natural product discovery and pathway dissection. Nat. Biotechnol. 26:225-233.
30. Ogasawara, Y., K. Katayama, A. Minami, M. Otsuka, T. Eguchi, and K. Kakinuma. 2004. Cloning, sequencing, and functional analysis of the biosynthetic gene cluster of macrolactam antibiotic vicenistatin in Streplomyces halstedii. Chem. Biol. 11:79-86. (Pubitemid 38203992)
31. Piel, J., D. Hui, N. Fusetani, and S. Matsunaga. 2004. Targeting modular polyketide synthases with iteratively acting acyltransferases from metagenomes of uncultured bacterial consortia. Environ. Microbiol. 6:921-927.
32. Piel, J., G. Wen, M. Platzer, and D. Hui. 2004. Unprecedented diversity of catalytic domains in the first four modules of the putative pederin polyketide synthase. Chembiochem 5:93-98. (Pubitemid 38095026)
33. Reger, A. S., J. M. Carney, and A. M. Gulick. 2007. Biochemical and crystallographic analysis of substrate binding and conformational changes in acetyl-CoA synthetase. Biochemistry 46:6536-6546.
34. Ridley, C. P., H. Y. Lee, and C. Khosla. 2008. Evolution of polyketide synthases in bacteria. Proc. Natl. Acad. Sci. U. S. A. 105:4595-4600.
35. Sekurova, O., H. Sletta, T. E. Ellingsen, S. Valla, and S. Zotchev. 1999. Molecular cloning and analysis of a pleiotropic regulatory gene locus from the nystatin producer Streptomyces noursei ATCC11455. FEMS Microbiol. Lett. 177:297-304.
36. Silakowski, B., G. Nordsiek, B. Kunze, H. Blöcker, and R. Müller. 2001. Novel features in a combined polyketide synthase/non- ribosomal peptide synthetase: the myxalamid biosynthetic gene cluster of the myxobacterium Stigmatella aurantiaca Sga15. Chem. Biol. 8:59-69. (Pubitemid 32165812)
37. Simunovic, V., J. Zapp, S. Rachid, D. Krug, P. Meiser, and R. Müller. 2006. Myxovirescin A biosynthesis is directed by hybrid polyketide synthases/non-ribosomal peptide synthetase, 3-hydroxy-3-methylglutaryl-CoA synthases, and trans-acting acyltransferases. Chembiochem. 7:1206-1220. (Pubitemid 44230844)
38. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
39. Tang, G.-L., Y.-Q. Cheng, and B. Shen. 2007. Chain initiation in the leinamycin-producing hybrid nonribosomal peptide/polyketide synthetase from Streptomyces atroolivaceus S-140. J. Biol. Chem, 282:20273-20282.
40. Thattai, M., Y. Burak, and B. I. Shraiman. 2007. The origins of specificity in polyketide synthase protein interactions. PLoS Comput. Biol. 3:1827-1835.
41. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
42. Traitcheva, N., H. Jenke-Kodama, J. He, E. Dittmann, and C. Hertweck. 2007. Non-colinear polyketide biosynthesis in the aureothin and neoaureothin pathways: an evolutionary perspective. Chembiochem 8:1841-1849. (Pubitemid 47612874)
43. Udwary, D. W., L. Zeigler, R. N. Asolkar, V. Singan, A. Lapidus, W. Fenical, P. R. Jensen, and B. S. Moore. 2007. Genome sequencing reveals complex secondary metabolome in the marine actinomycete Salinispora tropica. Proc. Natl. Acad. Sci. U. S. A. 104:10376-10381.
44. Zhang, X., and R. J. Parry. 2007. Cloning and characterization of the pyrrolomycin biosynthetic gene clusters from Aclinosporangium vitaminophilum ATCX 31673 and Streptomyces sp. strain UC 11065. Antimicrob. Agents Chemother. 51:946-957.
45. Zotchev, S., K. Haugan, O. Sekurova, II. Sletta, T. E. Ellingsen, and S. Valla. 2000. Identification of a gene cluster for antibacterial polyketide-derived antibiotic biosynthesis in the nystatin producer Streptomyces noursei ATCC 11455. Microbiology 146:611-619.