Identification and analysis of the paulomycin biosynthetic gene cluster and titer improvement of the paulomycins in Streptomyces paulus NRRL 8115

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Li, Jine ^a   Xie, Zhoujie ^a   Wang, Min ^a   Ai, Guomin ^a   Chen, Yihua ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSE; BACTERIAL PROTEIN; CARBOHYDRATES AND CARBOHYDRATE DERIVATIVES; CARBOXYLIC ACID; DIHYDRODIPICOLINATE REDUCTASE; ELONGATION FACTOR G; ENOYL REDUCTASE; GLYOXALASE; OXIDOREDUCTASE; PAULIC ACID; PAULOMENOL A PROTEIN; PAULOMENOL B PROTEIN; PAULOMYCIN A PROTEIN; PAULOMYCIN B PROTEIN; PAULOMYCIN PROTEIN; PAULOMYCIN RING A PROTEIN; PAULOMYCOSE; PYRANOSE OXIDASE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BIOSYNTHESIS; CONTROLLED STUDY; GENE CLUSTER; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PAU10 GENE; PAU11 GENE; PAU12 GENE; PAU13 GENE; PAU14 GENE; PAU15 GENE; PAU16 GENE; PAU17 GENE; PAU18 GENE; PAU19 GENE; PAU20 GENE; PAU21 GENE; PAU22 GENE; PAU23 GENE; PAU24 GENE; PAU25 GENE; PAU26 GENE; PAU27 GENE; PAU32 GENE; PAU33 GENE; PAU36 GENE; PAU37 GENE; PAU4 GENE; PAU41 GENE; PAU42 GENE; PAU43 GENE; PAU44 GENE; PAU5 GENE; PAU6 GENE; PAU7 GENE; PROTEIN SYNTHESIS; STREPTOMYCES; STREPTOMYCES ALBUS; STREPTOMYCES PAULUS; GENETICS; MULTIGENE FAMILY;

STREPTOMYCES; STREPTOMYCES ALBUS; STREPTOMYCES SP.;

ANTI-BACTERIAL AGENTS; GENOME, BACTERIAL; MULTIGENE FAMILY; STREPTOMYCES;

EID: 84926312473     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120542     Document Type: Article

References (66)

1. Hopwood DA. Genetic contributions to understanding polyketide synthases. Chem Rev. 1977; 97: 2465-2497.
2. Winter JM, Tang Y. Synthetic biological approaches to natural product biosynthesis. Curr Opin Biotechnol. 2012; 23: 736-743. doi: 10.1016/j.copbio.2011.12.016 PMID: 22221832
3. Liu G, Chater KF, Chandra G, Niu G, Tan H. Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol Mol Biol Rev. 2013, 77: 112-143. doi: 10.1128/MMBR.00054-12 PMID: 23471619
4. Argoudelis AD, Brinkley TA, Brodasky TF, Buege JA, Meyer HF, et al. Paulomycins A and B. Isolation and characterization. J Antibiot (Tokyo). 1982; 35: 285-294. PMID: 7076577
5. Hanka LJ, Dietz A. U-43,120; a new antitumor antibiotic. I. Production, biological activity, microbiological assay and taxonomy of the producing microorganism. J Antibiot (Tokyo). 1976; 29: 611-617. PMID: 950315
6. Wiley PF. A new antibiotic, U-43,120 (NSC-163500). J Antibiot (Tokyo). 1976; 29: 587-589. PMID: 986384
7. Marshall VP, Little MS, Johnson LE. A new process and organism for the fermentation production of volonomycin. J Antibiot (Tokyo). 1981; 34: 902-904. PMID: 7287593
8. Baczynskyj L, Haak WJ, Knoll WM, Mizsak SA, Shilliday FB. New paulomycins produced by Streptomyces paulus. J Antibiot (Tokyo). 1988; 41:157-169. PMID: 3356604
9. Majer J, Chater KF. Streptomyces albus G produces an antibiotic complex identical to paulomycins A and B. J Gen Microbiol. 1987; 133: 2503-2507. PMID: 3448155
10. Braña AF, Rodríguez M, Pahari P, Rohr J, García LA, Blanco G. Activation and silencing of secondary metabolites in Streptomyces albus and Streptomyces lividans after transformation with cosmids containing the thienamycin gene cluster from Streptomyces cattleya. Arch Microbiol. 2014; 196: 345-355. doi: 10.1007/s00203-014-0977-z PMID: 24633227
11. Argoudelis AD, Baczynskyj L, Mizsak SA, Shilliday FB. O-demethylpaulomycins A and B, U-77,802 and U-77,803, paulomenols A and B, new metabolites produced by Streptomyces paulus. J Antibiot (Tokyo). 1988; 41: 1316-1330. PMID: 3192491
12. Mitscher LA, McCrae W, DeVoe SE, Shay AJ, Hausmann WK, Bohonos N. Senfolomycin A and B, new antibiotics. Antimicrob Agents Chemother. 1965; 5: 828-831. PMID: 5883505
13. Argoudelis AD, Baczynskyj L, Mizsak SA, Shilliday FB, Wiley PF. Structural relationships between senfolomycins and paulomycins. J Antibiot (Tokyo). 1988; 41: 1212-1222. PMID: 3141336
14. Argoudelis AD, Baczynskyj L, Mizsak SA, Shilliday FB, Spinelli PA, DeZwaan J. Paldimycins A and B and antibiotics 273a2 alpha and 273a2 beta. Synthesis and characterization. J Antibiot (Tokyo). 1987; 40: 419-436. PMID: 3294773
15. Argoudelis AD, Baczynskyj L, Haak WJ, Knoll WM, Mizsak SA, Shilliday FB. New paulomycins produced by Streptomyces paulus. J Antibiot (Tokyo). 1988; 41: 157-169. PMID: 3356604
16. Sanchez MS, Ford CW, Yancey RJ Jr. Evaluation of antibacterial agents in a high-volume bovine polymorphonuclear neutrophil Staphylococcus aureus intracellular killing assay. Antimicrob Agents Chemother. 1986; 29: 634-638. PMID: 2871811
17. Treating chlamydia infections with paulomycin. USA PatentWO 1988002630 A2; 1987.
18. Yang N. The study of bacteria diversity from the south China sea and Xinjiang desert and chemical investigation of one Streptomyces strain. Student PhD thesis: University of Chinese Academy of Sciences (China); 2014.
19. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. Practical Streptomyces genetics. Norwich: The John Innes Foundation; 2000.
20. Fernández E, Weissbach U, Sánchez Reillo C, Braña AF, Méndez C, Rohr J, et al. Identification of two genes from Streptomyces argillaceus encoding glycosyltransferases involved in transfer of a disaccharide during biosynthesis of the antitumor drug mithramycin. J Bacteriol. 1998; 180: 4929-4937. PMID: 9733697
21. Liu G, Tian Y, Yang H, Tan H. A pathway-specific transcriptional regulatory gene for nikkomycin biosynthesis in Streptomyces ansochromogenes that also influences colony development. Mol Microbiol. 2005; 55: 1855-1866. PMID: 15752205
22. Smanski MJ, Yu Z, Casper J, Lin S, Peterson RM, Chen Y, et al. Dedicated ent-kaurene and ent-atiserene synthases for platensimycin and platencin biosynthesis. Proc Natl Acad Sci USA. 2011; 108: 13498-13503. doi: 10.1073/pnas.1106919108 PMID: 21825154
23. rd ed. Cold Spring Laboratory, NY: Cold Spring Harbor Laboratory; 2001.
24. Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, et al. antiSMASH 2.0 - a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res. 2013; W204-W212.
25. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010; 11: 119. doi: 10.1186/1471-2105-11-119 PMID: 20211023
26. Liu Y, Li S, Zhang H, Wan Z, Zhang X, Du R. A one-step cloning method for the construction of somatic cell gene targeting vectors: application to production of human knockout cell lines. BMC Biotechnol. 2012; 12: 71. doi: 10.1186/1472-6750-12-71 PMID: 23046873
27. Treede I, Hauser G, Mühlenweg A, Hofmann C, Schmidt M, Weitnauer G, et al. Genes involved in formation and attachment of a two-carbon chain as a component of eurekanate, a branched-chain sugar moiety of avilamycin A. Appl Environ Microbiol. 2005; 71: 400-406. PMID: 15640214
28. Chen H, Guo Z, Liu HW. Biosynthesis of Yersiniose: Attachment of the two-carbon branched-chain is catalyzed by a thiamine pyrophosphate-dependent flavoprotein. J Am Chem Soc. 1998; 120: 11796-11797.
29. Olano C, García I, González A, Rodriguez M, Rozas D, Rubio J, et al. Activation and identification of five clusters for secondary metabolites in Streptomyces albus J1074. Microb Biotechnol. 2014; 7: 242-256. doi: 10.1111/1751-7915.12116 PMID: 24593309
30. Andersson A, Schneider G, Lindqvist Y. Purification and preliminary X-ray crystallographic studies of recombinant L-ribulose-5-phosphate 4-epimerase from Escherichia coli. Protein Sci. 1995; 4: 1648-1650. PMID: 8520491
31. Magarvey NA, Haltli B, He M, Greenstein M, Hucul JA. Biosynthetic pathway for mannopeptimycins, lipoglycopeptide antibiotics active against drug-resistant gram-positive pathogens. Antimicrob Agents Chemother. 2006; 50: 2167-2177. PMID: 16723579
32. rd ed. NY: Worth Publishers; 2000. p. 834.
33. Culbertson JE, Toney MD. Expression and characterization of PhzE from P. aeruginosa PAO1: aminodeoxyisochorismate synthase involved in pyocyanin and phenazine-1-carboxylate production. Biochim Biophys Acta. 2013; 1834: 240-246. doi: 10.1016/j.bbapap.2012.10.010 PMID: 23099261
34. Pierson LS 3rd, Pierson EA. Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl Microbiol Biotechnol. 2010; 86: 1659-1670. doi: 10.1007/s00253-010-2509-3 PMID: 20352425
35. Garrido LM, Lombó F, Baig I, Nur-E-Alam M, Furlan RL, Borda CC, et al. Insights in the glycosylation steps during biosynthesis of the antitumor anthracycline cosmomycin: characterization of two glycosyltransferase genes. Appl Microbiol Biotechnol. 2006; 73: 122-131. PMID: 16810496
36. Bretschneider T, Zocher G, Unger M, Scherlach K, Stehle T, Hertweck C. A ketosynthase homolog uses malonyl units to form esters in cervimycin biosynthesis. Nat Chem Biol. 2011; 8: 154-161. doi: 10.1038/nchembio.746 PMID: 22179067
37. Proschak A, Zhou Q, Schöner T, Thanwisai A, Kresovic D, Dowling A, et al. Biosynthesis of the insecticidal xenocyloins in Xenorhabdus bovienii. Chembiochem. 2014; 15: 369-372. doi: 10.1002/cbic.201300694 PMID: 24488732
38. Kwon HJ, Smith WC, Scharon AJ, Hwang SH, Kurth MJ, Shen B. C-O bond formation by polyketide synthases. Science. 2002; 297: 1327-1330. PMID: 12193782
39. Lin S, Van Lanen SG, Shen B. A free-standing condensation enzyme catalyzing ester bond formation in C-1027 biosynthesis. Proc Natl Acad Sci USA. 2009; 106: 4183-4188. doi: 10.1073/pnas.0808880106 PMID: 19246381
40. Bones AM, Rossiter JT. The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry. 2006; 67: 1053-1067. PMID: 16624350
41. Singh H, Dai Y, Outten FW, Busenlehner LS. Escherichia coli SufE sulfur transfer protein modulates the SufS cysteine desulfurase through allosteric conformational dynamics. J Biol Chem. 2013; 288: 36189-36200. doi: 10.1074/jbc.M113.525709 PMID: 24196966
42. Burns KE, Baumgart S, Dorrestein PC, Zhai H, McLafferty FW, Begley TP. Reconstitution of a new cysteine biosynthetic pathway in Mycobacterium tuberculosis. J Am Chem Soc. 2005; 127: 11602-11603. PMID: 16104727
43. Mihara H, Esaki N. Bacterial cysteine desulfurases: their function and mechanisms. Appl Microbiol Biotechnol. 2002; 60: 12-23. PMID: 12382038
44. Sasaki E, Zhang X, Sun HG, Lu MY, Liu TL, Ou A, et al. Co-opting sulphur-carrier proteins from primary metabolic pathways for 2-thiosugar biosynthesis. Nature. 2014; 510: 427-431. doi: 10.1038/nature13256 PMID: 24814342
45. Ikeda H, Nonomiya T, Usami M, Ohta T, Omura S. Organization of the biosynthetic gene cluster for the polyketide anthelmintic macrolide avermectin in Streptomyces avermitilis. Proc Natl Acad Sci USA. 1999; 96: 9509-9514. PMID: 10449723
46. Borisova SA, Zhao L, Melançon CE III, Kao CL, Liu HW. Characterization of the glycosyltransferase activity of desVII: analysis of and implications for the biosynthesis of macrolide antibiotics. J Am Chem Soc. 2004; 126: 6534-6535. PMID: 15161264
47. Borisova SA, Liu HW. Characterization of glycosyltransferase DesVII and its auxiliary partner protein DesVIII in the methymycin/picromycin biosynthetic pathway. Biochemistry. 2010; 49: 8071-8084. doi: 10.1021/bi1007657 PMID: 20695498
48. Rui Z, Petrícková K, Skanta F, Pospísil S, Yang Y, Chen CY, et al. Biochemical and genetic insights into asukamycin biosynthesis. J Biol Chem. 2010; 285: 24915-24924. doi: 10.1074/jbc.M110.128850 PMID: 20522559
49. Suzuki T, Mochizuki S, Yamamoto S, Arakawa K, Kinashi H. Regulation of lankamycin biosynthesis in Streptomyces rochei by two SARP genes, srrY and srrZ. Biosci Biotechnol Biochem. 2010; 74: 819-827. PMID: 20378964
50. Siitonen V, Claesson M, Patrikainen P, Aromaa M, Mäntsälä P, Schneider G, et al. Identification of latestage glycosylation steps in the biosynthetic pathway of the anthracycline nogalamycin. Chembiochem. 2012; 13: 120-128. doi: 10.1002/cbic.201100637 PMID: 22120896
51. Gao X, Tan CL, Yeo CC, Poh CL. Molecular and biochemical characterization of the xlnD-encoded 3-hydroxybenzoate 6-hydroxylase involved in the degradation of 2,5-xylenol via the gentisate pathway in Pseudomonas alcaligenes NCIMB 9867. J Bacteriol. 2005; 187: 7696-7702. PMID: 16267294
52. Silakowski B, Kunze B, Nordsiek G, Blöcker H, Höfle G, Müller R. The myxochelin iron transport regulon of the myxobacterium Stigmatella aurantiaca Sg a15. Eur J Biochem. 2000; 267: 6476-6485. PMID: 11029592
53. Palaniappan N, Kim BS, Sekiyama Y, Osada H, Reynolds KA. Enhancement and selective production of phoslactomycin B, a protein phosphatase IIa inhibitor, through identification and engineering of the corresponding biosynthetic gene cluster. J Biol Chem. 2003; 278: 35552-35557. PMID: 12819191
54. Kaysser L, Wemakor E, Siebenberg S, Salas JA, Sohng JK, Kammerer B, et al. Formation and attachment of the deoxysugar moiety and assembly of the gene cluster for caprazamycin biosynthesis. Appl Environ Microbiol. 2010; 76: 4008-4018. doi: 10.1128/AEM.02740-09 PMID: 20418426
55. Xue Y, Zhao L, Liu HW, Sherman DH. A gene cluster for macrolide antibiotic biosynthesis in Streptomyces venezuelae: architecture of metabolic diversity. Proc Natl Acad Sci USA. 1998; 95: 12111-12116. PMID: 9770448
56. Erb A, Luzhetskyy A, Hardter U, Bechthold A. Cloning and sequencing of the biosynthetic gene cluster for saquayamycin Z and galtamycin B and the elucidation of the assembly of their saccharide chains. Chembiochem. 2009; 10: 1392-1401. doi: 10.1002/cbic.200900054 PMID: 19384899
57. Thornalley PJ. Glyoxalase I - structure, function and a critical role in the enzymatic defence against glycation. Biochem Soc Trans. 2003; 31: 1343-1348. PMID: 14641060
58. Shen B, Hutchinson CR. Triple hydroxylation of tetracenomycin A2 to tetracenomycin C in Streptomyces glaucescens. Overexpression of the tcmG gene in Streptomyces lividans and characterization of the tetracenomycin A2 oxygenase. J Biol Chem. 1994; 269: 30726-30733. PMID: 7982994
59. Yan Y, Zhang L, Ito T, Qu X, Asakawa Y, Awakawa T, et al. Biosynthetic pathway for high structural diversity of a common dilactone core in antimycin production. Org Lett. 2012; 14: 4142-4145. doi: 10.1021/ol301785x PMID: 22861048
60. Huang SX, Lohman JR, Huang T, Shen B. A new member of the 4-methylideneimidazole-5-one-containing aminomutase family from the enediyne kedarcidin biosynthetic pathway. Proc Natl Acad Sci USA. 2013; 110: 8069-8074. doi: 10.1073/pnas.1304733110 PMID: 23633564
61. Girish TS, Navratna V, Gopal B. Structure and nucleotide specificity of Staphylococcus aureus dihydrodipicolinate reductase (DapB). FEMS Lett. 2011; 585: 2561-2567. doi: 10.1016/j.febslet.2011.07.021 PMID: 21803042
62. Pang X, Aigle B, Girardet JM, Mangenot S, Pernodet JL, Decaris B, et al. Functional angucycline-like antibiotic gene cluster in the terminal inverted repeats of the Streptomyces ambofaciens linear chromosome. Antimicrob Agents Chemother. 2004; 48: 575-588. PMID: 14742212
63. Zhang YX, Denoya CD, Skinner DD, Fedechko RW, McArthur HA, Morgenstern MR, et al. Genes encoding acyl-CoA dehydrogenase (AcdH) homologues from Streptomyces coelicolor and Streptomyces avermitilis provide insights into the metabolism of small branched-chain fatty acids and macrolide antibiotic production. Microbiology. 1999; 145: 2323-2334. PMID: 10517585
64. Wu X, Flatt PM, Xu H, Mahmud T. Biosynthetic gene cluster of cetoniacytone A, an unusual aminocyclitol from the endosymbiotic Bacterium Actinomyces sp. Lu 9419. Chembiochem. 2009; 10: 304-314. doi: 10.1002/cbic.200800527 PMID: 19101977
65. Bihlmaier C, Welle E, Hofmann C, Welzel K, Vente A, Breitling E, et al. Biosynthetic gene cluster for the polyenoyltetramic acid alpha-lipomycin. Antimicrob Agents Chemother. 2006; 50: 2113-2121. PMID: 16723573
66. Singh S, Chang A, Helmich KE, Bingman CA, Wrobel RL, Beebe ET, et al. Structural and functional characterization of CalS11, a TDP-rhamnose 3′-O-methyltransferase involved in calicheamicin biosynthesis. ACS Chem Biol. 2013; 8: 1632-1639. doi: 10.1021/cb400068k PMID: 23662776