Naturally mosaic operons for secondary metabolite biosynthesis: variability and putative horizontal transfer of discrete catalytic domains of the epothilone polyketide synthase locus

Springer Science and Business Media LLC - Tập 270 - Trang 420-431 - 2003
J. V. Lopez1
1Division of Biomedical Marine Research, Harbor Branch Oceanographic Institution, Ft Pierce, USA

Tóm tắt

A putative instance of horizontal gene transfer (HGT) involving adjacent, discrete β-ketoacyl synthase (KS), acyl carrier protein (ACP) and nonribosomal peptide synthase (NRPS) domains of the epothilone Type I polyketide biosynthetic gene cluster from the myxobacterium Sorangium cellulosom was identified using molecular phylogenetics and sequence analyses. The specific KS domain of the module EPO B fails to cluster phylogenetically with other epothilone KS sequences present at this locus, in contrast to what is typically observed in many other Type I polyketide synthase (PKS) biosynthetic loci. Furthermore, the GC content of the epoB KS, epoA ACP and NRPS domains differs significantly from the base composition of other epothilone domain sequences. In addition, the putatively transferred epothilone loci are located near previously identified transposon-like sequences. Lastly, comparison with other KS loci revealed another possible case of horizontal transfer of secondary metabolite genes in the genus Pseudomonas. This study emphasizes the use of several lines of concordant evidence (phylogenetics, base composition, transposon sequences) to infer the evolutionary history of particular gene and enzyme sequences, and the results support the idea that genes coding for adaptive traits, e.g. defensive natural products, may be prone to transposition between divergent prokaryotic taxa and genomes.

Tài liệu tham khảo

Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–402 August PR, Tang L, Yoon YJ, Ning S, Muller R, Yu TW, Taylor M, Hoffman D, Kim CG, Zhang X (1998) Biosynthesis of the ansamycin antibiotic rifamycin: deductions from the molecular analysis of the rif biosynthetic gene cluster of Amycolatopsis mediterranei S699. Chem Biol 5:69–79 Avise JC, Ball RM (1990) Principles of genealogical concordance in species concepts and biological taxonomy. In: Futuyama D, Antonovics J (eds) Oxford surveys in evolutionary biology, vol 7. Oxford University Press, Oxford, pp 45–67 Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res 30:276–280 Bentley SD, et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147 Beyer S, Kunze B, Silakowski B, Muller R (1999) Metabolic diversity in myxobacteria—identification of the myxalamid and the stigmatellin biosynthetic gene cluster of Stigmatella aurantiaca Sg a15 and a combined polyketide-(poly) peptide gene cluster from the epothilon producing strain Sorangium cellulosum So ce90. Biochim Biophys Acta 1445:185 −195 Blot M (1994) Transposable elements and adaptation of host bacteria. Genetica 93:5–12 Brown EW, LeClerc JE, Kotewicz ML, Cebula TA (2001) The three R’s of bacterial evolution: how replication, repair, and recombination frame the origin of species. Environ Mol Mutagen 38:248–260 Chadwick DJ, Whelan J (eds) (1992) Secondary metabolites: their function and evolution (Ciba Foundation Symposium). Wiley, Chichester Charity JC, Pak K, Delwiche CF, Hutcheson SW (2003) Novel exchangeable effector loci associated with the Pseudomonas syringae hrp pathogenicity island: evidence for integron-like assembly from transposed gene cassettes. Mol Plant Microbe Interact 16:495–507 Donadio S, Katz L (1992) Organization of the enzymatic domains in the multifunctional polyketide synthase involved in erythromycin formation in Saccharopolyspora erythraea. Gene 111:51–60 Du L, Shen B (2001) Biosynthesis of hybrid peptide-polyketide natural products. Curr Opin Drug Disc Dev 4:215–228 Du L, Sanchez C, Chen M, Edwards DJ, Shen B (2000) The biosynthetic gene cluster for the antitumor drug bleomycin from Streptomyces verticillus ATCC15003 supporting functional interactions between nonribosomal peptide synthetases and a polyketide synthase. Chem Biol 7:623–642 Eisen J (2000) Horizontal gene transfer among microbial genomes: new insights from complete genome analysis. Curr Opin Genet Dev 10:606–611 Gonnet GH, Benner SA (1991) Computational biochemistry research at ETH. (Technical Report 154, Departement Informatik, Eidgenössische Technische Hochschule, Zürich) Graur D, Li WH (1997) Fundamentals of molecular evolution. Sinauer, Sunderland, Mass. Haydock SF, Aparicio JF, Molnar I, Schwecke T, Khaw LE, Konig A, Marsden AF, Galloway IS, Staunton J, Leadlay PF (1995) Divergent sequence motifs correlated with the substrate specificity of (methyl) malonyl-CoA:acyl carrier protein transacylase domains in modular polyketide synthases. FEBS Lett 374:246–248 Henikoff S, Henikoff JG (1992) Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89:10915–10919 Hopwood DA (1997) Genetic contributions to understanding polyketide synthases. Chem Rev 97:2465–2497 Hopwood DA, Sherman DH (1990) Molecular genetics of polyketides and its comparison to fatty acid biosynthesis. Annu Rev Genet 24:37–66 Huang G, Zhang L, Birch RG (2001) A multifunctional polyketide-peptide synthetase essential for albicidin biosynthesis in Xanthomonas albilineans. Microbiology 147:631–642 Jain R, Rivera MC, Moore JE, Lake JA (2002) Horizontal gene transfer in microbial genome evolution. Theor Popul Biol 61:489–495 Khosla C, Gokhale RS, Jacobsen JR, Cane DE (1999) Tolerance and specificity of polyketide synthases. Annu Rev Biochem 68:219–253 Koonin EV, Makarova KS, Aravind L (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55:709–742 Lan R, Reeves PR (1996) Gene transfer is a major factor in bacterial evolution. Mol Biol Evol 13:47–55 Lawrence JG (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 95:9413–9417 Lawrence JG, Roth JR (1996) Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics 143:1843–1860. Liisa BK, LB, Morton, RA, Golding GB (2001) Codon bias and base composition are poor indicators of horizontally transferred genes. Mol Biol Evol 18:404–412 Longley RE, Gunasekera SP, Faherty D, Mclane J, Dumont F (1993) Immunosuppression by discodermolide. Ann NY Acad Sci 696:94–107 Marahiel MA, Stachelhaus T, Mootz HD (1997) Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem Rev 97:2651–2673 McInerney JO (1998) GCUA: General Codon Usage Analyses. Bioinform Appl Notes 14:372–373 Moffit MC, Neilan BA (2003) Evolutionary affiliations within the superfamily of ketosynthases reflect complex pathway associations. J Mol Evol 56:446–457 Molnar I, et al (2000) The biosynthetic gene cluster for the microtubule-stablizing agents epothilones A and B from Sorangium cellusom So ce90. Chem Biol 7:97–109 Motamedi H, Cai S-J, Shafiee A, Elliston KO (1997) Structural organization of a multifunctional polyketide synthase involved in the biosynthesis of the macrolide immunosuppressant FK506. Eur J Biochem 244:74–80 Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, Oxford Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304 Ohno S (1970) Evolution by gene duplication. Springer-Verlag, New York Omura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, Takahashi Y, Horikawa H, Nakazawa H, Osonoe T, Kikuchi H, Shiba T, Sakaki Y, Hattori M (2001) Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci USA 98:12215–12220 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 Romero D, Palacios R (1997) Gene amplification and genomic plasticity in prokaryotes. Annu Rev Genet 31:91–111 Silakowski B, Kunze B, Muller R (2001) Multiple hybrid polyketide synthase/non-ribosomal peptide synthetase gene clusters in the myxobacterium Stigmatella aurantiaca. Gene 275:233–240 Snyder RV, Gibbs PDL, Palacios A, Abiy L, Dickey R, Lopez JV, Rein KS (2003) Polyketide synthase genes from marine dinoflagellates. Marine Biotechnol 5:1–12 Sosio M, Bossi E, Bianci A, Donadio S (2000) Multiple peptide synthetase gene clusters in Actinomycetes. Mol Gen Genet 264:213–221 Staunton J, Weissman KJ. (2001) Polyketide biosynthesis: a millennium review. Natural Prod Rep 18:380–416 Stone MJ, Williams DH (1992) On the evolution of functional secondary metabolites (natural products). Mol Microbiol 6:29–34 Strimmer K, von Haeseler A (1996) Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969 Sueoka N (1992) Directional mutation pressure, selective constraints, and genetic equilibria. J Mol Evol 34:95–114 Suzuki Y, Gojobori T (1999) A method for detecting positive selection at single amino acid sites. Mol Biol Evol 16:1315–1328 Swofford DL (2001) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods), Version 4. Sinauer, Sunderland, Mass. Tang L, Shah S, Chung L, Carney J, Katz L, Khosla C, Julien B (2000) Cloning and heterologous expression of the epothilone gene cluster. Science 287:640–642 Thompson JD, Higgins D, Gibson TJ (1994) CLUSTAL version W: a novel multiple sequence alignment program. Nucleic Acids Res 22:4673–4680. Tsoi CJ, Khosla C (1995) Combinatorial biosynthesis of ‘unnatural’ natural products: the polyketide example. Chem Biol 2:355–362 Underwood AJ (1998) Experiments in ecology. Cambridge University Press, London Wagner A (2002) Selection and gene duplication: a view from the genome. Genome Biol 3:1012.1–1012.3 Walton JD (2000) Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: a hypothesis. Fungal Genet Biol 30:167–171 Wiener P, Egan S, Wellington EM (1998) Evidence for transfer of antibiotic-resistance genes in soil populations of streptomycetes. Mol Ecol 7:1205–1216 Zgur-Bertok D (1999) Mechanisms of horizontal gene transfer. Folia Biol (Praha) 45:91–96