Type I polyketide synthases may have evolved through horizontal gene transfer.

GINOLHAC, Aurélien; Jarrin, Cyrille; Robe, Patrick; Perrière, Guy; Vogel, Timothy M; Simonet, Pascal; Nalin, Renaud

doi:10.1007/s00239-004-0161-1

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Article (Scientific journals)

Type I polyketide synthases may have evolved through horizontal gene transfer.

GINOLHAC, Aurélien; Jarrin, Cyrille; Robe, Patrick et al.

2005 • In Journal of Molecular Evolution, 60 (6), p. 716-25

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https://hdl.handle.net/10993/58146

DOI
10.1007/s00239-004-0161-1

PubMed
15909225

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Keywords :

Bacterial Proteins; Macrolides; soraphen A; Nystatin; Polyketide Synthases; 7XU7A7DROE (Amphotericin B); 8O0C852CPO (Natamycin); EC 2.3.- (Acyltransferases); Acyltransferases/genetics; Amphotericin B/pharmacology; Bacterial Proteins/metabolism; Evolution, Molecular; Gene Transfer Techniques; Gene Transfer, Horizontal; Genes, Bacterial; Macrolides/pharmacology; Models, Genetic; Multigene Family; Natamycin/pharmacology; Nystatin/pharmacology; Phylogeny; Polyketide Synthases/chemistry/metabolism; Protein Structure, Tertiary

Abstract :

[en] Type I polyketide synthases (PKSI) are modular multidomain enzymes involved in the biosynthesis of many natural products of industrial interest. PKSI modules are minimally organized in three domains: ketosynthase (KS), acyltransferase (AT), and acyl carrier protein. The KS domain phylogeny of 23 PKSI clusters was determined. The results obtained suggest that many horizontal transfers of PKSI genes have occurred between actinomycetales species. Such gene transfers may explain the homogeneity and the robustness of the actinomycetales group since gene transfers between closely related species could mimic patterns generated by vertical inheritance. We suggest that the linearity and instability of actinomycetales chromosomes associated with their large quantity of genetic mobile elements have favored such horizontal gene transfers.

Disciplines :

Biotechnology

Author, co-author :

GINOLHAC, Aurélien

Jarrin, Cyrille

Robe, Patrick

Perrière, Guy

Vogel, Timothy M

Simonet, Pascal

Nalin, Renaud

External co-authors :

Language :

English

Title :

Type I polyketide synthases may have evolved through horizontal gene transfer.

Publication date :

June 2005

Journal title :

Journal of Molecular Evolution

ISSN :

0022-2844

eISSN :

1432-1432

Publisher :

Springer, United States - Delaware

Volume :

Issue :

Pages :

716-25

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBilu :

since 29 November 2023

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Bibliography

Y Anzai N Saito M Tanaka K Kinoshita Y Koyama K Kato 2003 Organization of the biosynthetic gene cluster for the polyketide macrolide mycinamicin in Micromonospora griseorubida FEMS Microbiol Lett 218 135 341
JF Aparicio R Fouces MV Mendes N Olivera JF Martin 2000 A complex multienzyme system encoded by five polyketide synthase genes is involved in the biosynthesis of the 26-membered polyene macrolide pimaricin in Streptomyces natalensis Chem Biol 7 895 905
SD Bentley S Brown LD Murphy DE Harris MA Quail J Parkhill BG Barrell JR McCormick RI Santamaria R Losick M Yamasaki H Kinashi CW Chen G Chandra D Jakimowicz HM Kieser T Kieser KF Chater 2004 SCP1, a 356 023 bp linear plasmid adapted to the ecology and developmental biology of its host, Streptomyces coelicolor A3(2) Mol Microbiol 51 1615 1628
T Brautaset ON Sekurova H Sletta TE Ellingsen AR Strom S Valla SB Zotchev 2000 Biosynthesis of the polyene antifungal antibiotic nystatin in Streptomyces noursei ATCC 11455: analysis of the gene cluster and deduction of the biosynthetic pathway Chem Biol 7 395 403
P Caffrey S Lynch E Flood S Finnan M Oliynyk 2001 Amphotericin biosynthesis in Streptomyces nodosus Deductions from analysis of polyketide synthase and late genes. Chem Biol 8 713 723
GL Challis DA Hopwood 2003 Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species Proc Natl Acad Sci USA 100 14555 14561
CW Chen CH Huang HH Lee HH Tsai R Kirby 2002 Once the circle has been broken: dynamics and evolution of Streptomyces chromosomes Trends Genet 18 522 529
J Cortes SF Haydock GA Roberts DJ Bevitt PF Leadlay 1990 An unusually large multifunctional polypeptide in the erythromycin-producing polyketide synthase of Saccharopolyspora erythraea Nature 348 176 178
E Cundliffe N Bate A Butler S Fish A Gandecha L Merson- Davies 2001 The tylosin-biosynthetic genes of Streptomyces fradiae Antonie Van Leeuwenhoek 79 229 234
L Du C Sanchez B Shen 2001 Hybrid peptide-polyketide natural products: biosynthesis and prospects toward engineering novel molecules Metab Eng 3 78 95
S Egan P Wiener D Kallifidas EM Wellington 2001 Phylogeny of Streptomyces species and evidence for horizontal transfer of entire and partial antibiotic gene clusters Antonie Van Leeuwenhoek 79 127 133
Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle
N Gaitatzis B Silakowski B Kunze G Nordsiek H Blocker G Hofle R Muller 2002 The biosynthesis of the aromatic myxobacterial electron transport inhibitor stigmatellin is directed by a novel type of modular polyketide synthase J Biol Chem 277 13082 13090
N Galtier M Gouy C Gautier 1996 SEAVIEW and PHYLO_ WIN: two graphic tools for sequence alignment and molecular phylogeny Comput Appl Biosci 12 543 548
JP Gogarten WF Doolittle JG Lawrence 2002 Prokaryotic evolution in light of gene transfer Mol Biol Evol 19 2226 2238
RS Gokhale C Khosla 2000 Role of linkers in communication between protein modules Curr Opin Chem Biol 4 22 27
S Guindon O Gascuel 2003 A simple, fast, and accurate algorithm to estimate large phytogenies by maximum likelihood Syst Biol 52 696 704
D Hoffmann JM Hevel RE Moore BS Moore 2003 Sequence analysis and biochemical characterization of the nostopeptolide A biosynthetic gene cluster from Nostac sp. GSV224 Gene 311 171 180
DA Hopwood 1997 Genetic contributions to understanding polyketide synthases Chem Rev 97 2465 2497
H Ikeda T Nonomiya M Usami T Ohta S Omura 1999 Organization of the biosynthetic gene cluster for the polyketide anthelmintic macrolide avermectin in Streptomyces avermitilis Proc Natl Acad Sci USA 96 9509 9514
GA Jenkin TP Stinear PDR Johnson JK Davies 2003 Subtractive hybridization reveals a type I polyketide synthase locus specific to Mycobacterium ulcerans J Bacteriol 185 6870 6882
DT Jones WR Taylor JM Thornton 1992 The rapid generation of mutation data matrices from protein sequences CABIOS 8 275 282
SJ Kakavas L Katz D Stassi 1997 Identification and characterization of the niddamycin polyketide synthase genes from Streptomyces caelestis J Bacteriol 179 7515 7522
H Kishino M Hasegawa 1989 Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea J Mol Evol 29 170 179
CG Kurland B Canback OG Berg 2003 Horizontal gene transfer: a critical view Proc Natl Acad Sci USA 100 9658 9662
JG Lawrence JR Roth 1996 Selfish operon theory: Horizontal gene transfer may drive the evolution of gene clusters Genetics 143 1843 1860
J Ligon S Hill J Beck R Zirkle I Molnar J Zawodny S Money T Schupp 2002 Characterization of the biosynthetic gene cluster for the antifungal polyketide soraphen A from Sorangium cellulosum So ce26 Gene 285 257 267
F Lombó AF Braña C Méndez JA Salas 1999 The mithramycin gene cluster of Streptomyces argillaceus contains a positive regulatory gene and two repeated DNA sequences that are located at both ends of the cluster J Bacteriol 181 642 647
JV Lopez 2003 Naturally mosaic operons for secondary metabolite biosynthesis; variability and putative horizontal transfer of discrete catalytic domains of the epothilone polyketide synthase locus Mol Gen Genomics 270 420 431
S Mochizuki K Hiratsu M Suwa T Ishii F Sugino K Yamada H Kinashi 2003 The large linear plasmid pSLA2-L of Streptomyces rochei has an unusually condensed gene organization for secondary metabolism Mol Microbiol 48 1501 1510
MC Moffitt BA Neilan 2003 Evolutionary affiliations within the superfamily of ketosynthases reflect complex pathway associations J Mol Evol 56 446 457
I Molnar T Schupp M Ono R Zirkle M Milnamow B Nowak-Thompson N Engel C Toupet A Stratmann DD Cyr J Gorlach JM Mayo A Hu S Goff J Schmid JM Ligon 2000 The biosynthetic gene cluster for the microtubule-stabilizing agents epothilones A and B from Sorangium cellulosum So ce90 Chem Biol 7 97 109
B Nowak-Thompson SJ Gould JE Loper 1997 Identification and sequence analysis of the genes encoding a polyketide synthase required for pyoluteorin biosynthesis in Pseudomonas fluorescens Pf-5 Gene 204 17 24
G Perrière M Gouy 1996 WWW-Query: an on-line retrieval system for biological sequence banks Biochimie 78 364 369
M Robinson-Rechavi D Huchon 2000 RRTree: Relative-rate tests between groups of sequences on a phylogenetic tree Bioinformatics 16 296 297
T Schupp C Toupet B Cluzel S Neff S Hill JJ Beck JM 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
T Schwecke JF Aparicio I Molnar A Konig LE Khaw SF Haydock M Oliynyk P Caffrey J Cortes JB Lester GA Bohm J Stauton PF Leadlay 1995 The biosynthetic gene cluster for the polyketide immunosuppressant rapamycin Proc Natl Acad Sci USA 92 7839 7843
S Shah Q Xue L Tang JR Carney M Betlach R McDaniel 2000 Cloning, characterization and heterologous expression of a polyketide synthase and P-450 oxidase involved in the biosynthesis of the antibiotic oleandomycin J Antibiot 53 502 508
B Shen 2003 Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms Curr Opin Chem Biol 7 285 295
B Silakowski HU Schairer H Ehret B Kunze S Weinig G Nordsiek P Brandt H Blocker G Hofle S Beyer R Muller 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
B Silakowski G Nordsiek B Kunze H Blocker R Muller 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
J Staunton KJ Weissman 2001 Polyketide biosynthesis: a millennium review Nat Prod Rep 18 380 416
TP Stinear A Mve-Obiang PLC Small W Frigui MJ Pryor R Brosch GA Jenkin PDR Johnson JK Davies RE Lee S Adusumilli T Gamier SF Haydock PF Leadlay ST Cole 2004 Giant plasmid-encoded polyketide synthases produce the macrolide toxin of Mycobacterium ulcerans Proc Natl Acad Sci USA 101 1345 1349
J Stonesifer P Matsushima RH Baltz 1986 High frequency conjugal transfer of tylosin genes and amplifiable DNA in Streptomyces fradiae Mol Gen Genet 202 348 355
L Tang YJ Yoon CY Choi CR Hutchinson 1998 Characterization of the enzymatic domains in the modular polyketide synthase involved in rifamycin B biosynthesis by Amycolatopsis mediterranei Gene 216 255 265
CJ Thompson D Fink LD Nguyen 2002 Principles of microbial alchemy: insights from the Streptomyces coelicolor genome sequence Genome Biol 3 1 4
JD Thompson F Plewniak J-C Thierry O Poch 2000 DbClustal: rapid and reliable global multiple alignments of protein sequences detected by database searches Nucleic Acids Res 28 2919 2926
D Tillett E Dittmann M Erhard H von Dohren T Borner BA Neilan 2000 Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system Chem Biol 7 753 764
V Torsvik L Ovreas TF Thingstad 2002 Prokaiyotic Diversity-Magnitude, dynamics, and controlling factors Science 296 1064 1066
Y Volchegursky Z Hu L Katz R McDaniel 2000 Biosynthesis of the anti-parasitic agent megalomicin: transformation of erythromycin to megalomicin in Saccharopolyspora erythraea Mol Microbiol 37 752 762
C Waldron P Matsushima PR Rosteck Jr MC Broughton J Turner K Madduri KP Crawford DJ Merlo RH Baltz 2001 Cloning and analysis of the spinosad biosynthetic gene cluster of Saccharopolyspora spinosa Chem Biol 8 487 499
K Watanabe CCC Wang CN Boddy DE Cane C Khosla 2003 Understanding substrate specificity of polyketide synthase modules by generating hybrid multimodular synthases J Biol Chem 278 42020 42026
D Weaver N Karoonuthaisiri HH Tsai CH Huang ML Ho S Gai KG Patel J Huang SN Cohen DA Hopwood CW Chen CM Kao 2004 Genome plasticity in Streptomyces: identification of 1 Mb TIRs in the S. coelicolor A3(2) chromosome Mol Microbiol 51 1535 1550
T Weber K Welzel S Pelzer A Vente W Wohlleben 2003 Exploiting the genetic potential of polyketide producing Streptomyces J Biotechnol 106 221 223
P Wiener S Egan MH Wellington 1998 Evidence for transfer of antibiotic-resistance genes in soil populations of Streptomycetes Mol Ecol 7 1205 1216
K Wu L Chung P Revill L Katz CD Reeves 2000 The FK520 gene cluster of Streptomyces hygroscopicus var. ascomyceticus (ATCC 14891) contains genes for biosynthetis of unusual polyketide extender units Gene 251 81 90
Y Xue D Wilson DH Sherman 2000 Genetic architecture of the polyketide synthases for methymycin and pikromycin series macrolides Gene 245 203 211
G Yadav RS Gokhale D Mohanty 2003 Computational approach for prediction of domain organization and substrate specificity of modular polyketide synthases J Mol Biol 328 335 363
M Yamasaki Y Ikuto A Ohira K Chater H Kinashi 2003 Limited regions of homology between linear and circular plasmids encoding methylenomycin biosynthesis in two independently isolated streptomycetes Microbiology 149 1351 1356
G Zhu MJ LaGier F Stejskal JJ Millership X Cai JS Keithly 2002 Cryptosporidium parvum: the first protist known to encode a putative polyketide synthase Gene 298 79 89