Evolutionary implications of bacterial polyketide synthases

Molecular Biology and Evolution

Volumn 22, Issue 10, 2005, Pages 2027-2039

  Jenke Kodama, Holger ^a   Sandmann, Axel ^b   Müller, Rolf ^b   Dittmann, Elke ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

Bayesian analysis; Fatty acid synthases; Multimodular enzymes; Polyketides; Secondary metabolites

Indexed keywords

ACYLTRANSFERASE; BACTERIAL ENZYME; FATTY ACID SYNTHASE; GLYCOLIPID; MYCOLIC ACID; POLYKETIDE SYNTHASE; POLYUNSATURATED FATTY ACID;

ACTINOBACTERIA; ARTICLE; BACTERIAL GENOME; BACTERIUM; BIOSYNTHESIS; DATA BASE; FUNGUS; GENE DUPLICATION; GENE SEQUENCE; GENE TRANSFER; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; BACTERIA; BACTERIAL PROTEINS; GENOME, BACTERIAL; PHYLOGENY; POLYKETIDE SYNTHASES; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

ACTINOBACTERIA; ACTINOBACTERIA (CLASS); ANIMALIA; CYANOBACTERIA; FUNGI; PROTEOBACTERIA;

EID: 24744433982     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msi193     Document Type: Article

References (55)

1. Bender, C. L., F. Alarcon-Chaidez, and D. C. Gross. 1999. Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. 63:266-292.
2. Black, T. A., and C. P. Wolk. 1994. Analysis of a Het- mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing. J. Bacteriol. 176:2282-2292.
3. Bode, H. B., and R. Müller. 2003. Possibility of bacterial recruitment of plant genes associated with the biosynthesis of secondary metabolites. Plant Physiol. 132:1153-1161.
4. _. 2005. The impact of bacterial genomics on natural product research. Angew. Chem. Int. Ed. Engl. (in press).
5. Brennan, P. J., and H. Nikaido. 1995. The envelope of mycobacteria. Annu. Rev. Biochem. 64:29-63.
6. Brochier, C., E. Bapteste, D. Moreira, and H. Philippe. 2002. Eubacterial phylogeny based on translational apparatus proteins. Trends Genet. 18:1-5.
7. Campbell, E. L., M. F. Cohen, and J. C. Meeks. 1997. A polyketide-synthase-like gene is involved in the synthesis of heterocyst glycolipids in Nostoc punctiforme strain ATCC 29133. Arch. Microbiol. 167:251-258.
8. Cerda-Olmedo, E. 1994. The genetics of chemical diversity. Crit. Rev. Microbiol. 20:151-160.
9. Cole, S. T., R. Brosch, J. Parkhill et al. (42 co-authors). 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
10. Crosa, J. H., and C. T. Walsh. 2002. Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol. Mol. Biol. Rev. 66:223-249.
11. Dobrindt, U., B. Hochhut, U. Hentschel, and J. Hacker. 2004. Genomic islands in pathogenic and environmental microorganisms. Nat. Rev. Microbiol. 2:414-424.
12. 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 252:675-679.
13. Duitman, E. H., L. W. Hamoen, M. Rembold et al (13 co-authors). 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. USA 96:13294-13299.
14. Firn, R. D., and C. G. Jones. 2000. The evolution of secondary metabolism - a unifying model. Mol. Microbiol. 37:989-994.
15. Gaitatzis, N., A. Hans, R. Müller, and S. Beyer. 2001. The mtaA gene of the myxothiazol biosynthetic gene cluster from Stigmatella aurantiaca DW4/3-1 encodes a phosphopantetheinyl transferase that activates polyketide synthases and polypeptide synthetases. J. Biochem. (Tokyo) 129:119-124.
16. Gamieldien, J., A. Ptitsyn, and W. Hide. 2002. Eukaryotic genes in Mycobacterium tuberculosis could have a role in pathogenesis and immunomodulation. Trends Genet. 18:5-8.
17. Gehring, A. M., S. T. Wang, D. B. Kearns, N. Y. Storer, and R. Losick. 2004. Novel genes that influence development in Streptomyces coelicolor. J. Bacteriol. 186:3570-3577.
18. He, J., and C. Hertweck. 2003. Iteration as programmed event during polyketide assembly; molecular analysis of the aureothin biosynthesis gene cluster. Chem. Biol. 10:1225-1232.
19. Huelsenbeck, J. P. 2000. MrBayes: Bayesian inference of phylogeny. Distributed by the author.
20. Jones, C. G., and R. D. Firn. 1991. On the evolution of plant secondary metabolite chemical diversity. Phil. Trans. R. Soc. Lond. B Biol. Sci. 333:273-280.
21. Jones, D. T., W. R. Taylor, and J. M. Thornton. 1992. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8:275-282.
22. Kao, C. M., R. Pieper, D. E. Cane, and C. Khosla. 1996. Evidence for two catalytically independent clusters of active sites in a functional modular polyketide synthase. Biochemistry 35:12363-12368.
23. Kikuchi, S., D. L. Rainwater, and P. E. Kolattukudy. 1992. Purification and characterization of an unusually large fatty acid synthase from Mycobacterium tuberculosis var. bovis BCG. Arch. Biochem. Biophys. 295:318-326.
24. Kroken, S., N. L. Glass, J. W. Taylor, O. C. Yoder, and B. G. Turgeon. 2003. Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc. Natl. Acad. Sci. USA 100:15670-15675.
25. Lawrence, J. G., and H. Ochman. 1997. Amelioration of bacterial genomes: rates of change and exchange. J. Mol. Evol. 44:383-397.
26. Liu, W., S. D. Christenson, S. Standage, and B. Shen. 2002. Biosynthesis of the enediyne antitumor antibiotic C-1027. Science 297:1170-1173.
27. Liu, W., K. Nonaka, L. Nie et al. (11 co-authors). 2005. The neocarzinostatin biosynthetic gene cluster from Streptomyces carzinostaticus ATCC 15944 involving two iterative type I polyketide synthases. Chem. Biol. 12:293-302.
28. Maddison, W. R., and W. P. Maddison. 2000. MacClade. Version 4.0. Sinauer Associates, Sunderland, Mass.
29. McCarthy, A. D., and D. G. Hardie. 1984. Fatty acid synthase - an example of protein fusion by gene fusion. Trends Biochem. Sci. 9:60-63.
30. McGuffin, L. J., K. Bryson, and D. T. Jones. 2000. The PSIPRED protein structure prediction server. Bioinformatics 16:404-405.
31. Meeks, J. C., E. L. Campbell, M. L. Summers, and F. C. Wong. 2002. Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch. Microbiol. 178:395-403.
32. Metz, J. G., P. Roessler, D. Facciotti et al. (13 co-authors). 2001. Production of polyunsaturated fatty acids by polyketide synthases in both prokaryotes and eukaryotes. Science 293:290-293.
33. Miller, D. A., L. Luo, N. Hillson, T. A. Keating, and C. T. Walsh. 2002. Yersiniabactin synthetase: a four-protein assembly line producing the nonribosomal peptide/polyketide hybrid siderophore of Yersinia pestis. Chem. Biol. 9:333-344.
34. Moche, M., G. Schneider, P. Edwards, K. Dehesh, and Y. Lindqvist. 1999. Structure of the complex between the antibiotic cerulenin and its target, beta-ketoacyl-acyl carrier protein synthase. J. Biol. Chem. 274:6031-6034.
35. Moss, S. J., C. J. Martin, and B. Wilkinson. 2004. Loss of co-linearity by modular polyketide synthases: a mechanism for the evolution of chemical diversity. Nat. Prod. Rep. 21: 575-593.
36. Ohnishi, Y., S. Kameyama, H. Onaka, and S. Horinouchi. 1999. The A-factor regulatory cascade leading to streptomycin biosynthesis in Streptomyces griseus: identification of a target gene of the A-factor receptor. Mol. Microbiol. 34:102-111.
37. Paitan, Y., G. Alon, E. Orr, E. Z. Ron, and E. Rosenberg. 1999. The first gene in the biosynthesis of the polyketide antibiotic TA of Myxococcus xanthus codes for a unique PKS module coupled to a peptide synthetase. J. Mol. Biol. 286:465-474.
38. Pereto, J., P. Lopez-Garcia, and D. Moreira. 2004. Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem. Sci. 29:469-477.
39. Piel, J. 2002. A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles. Proc. Natl. Acad. Sci. USA 99:14002-14007.
40. 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.
41. Ragan, M. A. 2001. Detection of lateral gene transfer among microbial genomes. Curr. Opin. Genet. Dev. 11:620-626.
42. Schweizer, E., and J. Hofmann. 2004. Microbial type I fatty acid synthases (FAS): major players in a network of cellular FAS systems. Microbiol. Mol. Biol. Rev. 68:501-517.
43. Serre, L., E. C. Verbree, Z. Dauter, A. R. Stuitje, and Z. S. Derewenda. 1995. The E. coli malonyl-CoA: acyl carrier protein transacylase at 1.5 A resolution. Crystal structire of a FAS component. J. Biol. Chem. 270:12961-12964.
44. Shen, B., L. Du, C. Sanchez, D. J. Edwards, M. Chen, and J. M. Murrell. 2001. The biosynthetic gene cluster for the anticancer drug bleomycin from Streptomyces verticillus ATCC15003 as a model for hybrid peptide-polyketide natural product biosynthesis. J. Ind. Microbiol. Biotechnol. 27:378-385.
45. Silakowski, B., H. U. Schairer, H. Ehret et al. (11 co-authors). 1999. New lessons for combinatorial biosynthesis from myxobacteria. The myxothiazol biosynthetic gene cluster of Stigmatella aurantiaca DW4/3-1. J. Biol. Chem. 274: 37391-37399.
46. Smith, G. R. 1991. Conjugational recombination in E. coli: myths and mechanisms. Cell 64:19-27.
47. Staunton, J., and K. J. Weissman. 2001. Polyketide biosynthesis: a millennium review. Nat. Prod. Rep. 18:380-416.
48. Tang, G. L., Y. Q. Cheng, and B. Shen. 2004. Leinamycin biosynthesis revealing unprecedented architectural complexity for a hybrid polyketide synthase and nonribosomal peptide synthetase. Chem. Biol. 11:33-45.
49. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. ClustalW: improving the sensitivity of progressive multiple alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
50. Vissa, V. D., and P. J. Brennan. 2001. The genome of Mycobacterium leprae: a minimal mycobacterial gene set. Genome Biol. 2:REVIEWS1023.
51. Wallis, J. G., J. L. Watts, and J. Browse. 2002. Polyunsaturated fatty acid synthesis: what will they think of next? Trends Biochem. Sci. 27:467.
52. Weitnauer, G., A. Mühlenweg, A. Trefzer, D. Hoffmeister, R. D. Süssmuth, G. Jung, K. Welzel, A. Vente, U. Girreser, and A. Bechthold. 2001. Biosynthesis of the orthosomycin antibiotic avilamycin A: deductions from the molecular analysis of the avi biosynthetic gene cluster of Streptomyces viridochromogenes Tu57 and production of new antibiotics. Chem. Biol. 8:569-581.
53. Wenzel, S. C., B. Kunze, G. Hofle, B. Silakowski, M. Scharfe, H. Blocker, and R. Müller. 2005. Structure and biosynthesis of myxochromides S1-3 in Stigmatella aurantiaca: evidence for an iterative bacterial type I polyketide synthase and for module skipping in nonribosomal peptide biosynthesis. Chembiochem 6:375-385.
54. Woese, C. R. 1987. Bacterial evolution. Microbiol. Rev. 51:221-271.
55. Yadav, G., R. S. Gokhale, and D. Mohanty. 2003. SEARCHPKS: a program for detection and analysis of polyketide synthase domains. Nucleic Acids Res. 31:3654-3658.