Discovery of a new diol-containing polyketide by heterologous expression of a silent biosynthetic gene cluster from Streptomyces lavendulae FRI-5

Journal of Industrial Microbiology and Biotechnology

Volumn 45, Issue 2, 2018, Pages 77-87

  Pait, Ivy Grace Umadhay ^a   Kitani, Shigeru ^a   Roslan, Farah Wahidah ^a   Ulanova, Dana ^a,b   Arai, Masayoshi ^a   Ikeda, Haruo ^c   Nihira, Takuya ^a,d  

^a OSAKA UNIVERSITY   (Japan)

^b KOCHI UNIVERSITY   (Japan)

^c KITASATO UNIVERSITY   (Japan)

^d MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Genome mining; Heterologous expression; Polyketide; Silent secondary metabolites; Streptomyces

Indexed keywords

LAVENDIOL; POLYKETIDE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM CULTURE; BIOSYNTHESIS; CARBON NUCLEAR MAGNETIC RESONANCE; COLUMN CHROMATOGRAPHY; CONTROLLED STUDY; GENE CLUSTER; GENE FUNCTION; GENETIC ORGANIZATION; HETEROLOGOUS EXPRESSION; HETERONUCLEAR MULTIPLE BOND CORRELATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; INFRARED SPECTROSCOPY; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PROTON NUCLEAR MAGNETIC RESONANCE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SILENT GENE; STREPTOMYCES AVERMITILIS; STREPTOMYCES LAVENDULAE; CHEMISTRY; FUNGAL GENE; GENE EXPRESSION; GENETICS; METABOLISM; SECONDARY METABOLISM; STREPTOMYCES;

BIOSYNTHETIC PATHWAYS; GENE EXPRESSION; GENES, FUNGAL; POLYKETIDES; SECONDARY METABOLISM; STREPTOMYCES;

EID: 85038371680     PISSN: 13675435     EISSN: 14765535     Source Type: Journal    
DOI: 10.1007/s10295-017-1997-x     Document Type: Article

References (56)

1. Bachmann BO, Van Lanen SG, Baltz RH (2014) Microbial genome mining for accelerated natural products discovery: is a renaissance in the making? J Ind Microbiol Biotechnol 41:175–184. https://doi.org/10.1007/s10295-013-1389-9
2. Baltz RH (2016) Gifted microbes for genome mining and natural product discovery. J Ind Microbiol Biotechnol. https://doi.org/10.1007/s10295-016-1815-x
3. Bentley S, Chater K, Cerdeño-Tárraga A-M et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147. https://doi.org/10.1038/417141a
4. Bérdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are headin. J Antibiot (Tokyo) 65:441. https://doi.org/10.1038/ja.2012.54
5. Blin K, Medema MH, Kazempour D, Fischbach M, Breitling R, Takano E, Weber T (2013) antiSMASH 2.0-a versatile platform for genome mining of secondary metabolite producers. Nucl Acids Res 41:204–212. https://doi.org/10.1093/nar/gkt449
6. Bode HB, Bethe B, Höfs R, Zeeck A (2002) Big effects from small changes: possible ways to explore nature’s chemical diversity. ChemBioChem 3:619–627. https://doi.org/10.1002/1439-7633(20020703)3:7<619:AID-CBIC619>3.0.CO;2-9
7. Cane DE, He X, Kobayashi S, Omura S, Ikeda H (2006) Geosmin biosynthesis in Streptomyces avermitilis. Molecular cloning, expression, and mechanistic study of the germacradienol/geosmin synthase. J Antibiot (Tokyo) 59:471–479. https://doi.org/10.1038/ja.2006.66
8. Challis GL (2008) Mining microbial genomes for new natural products and biosynthetic pathways. Microbiology 154:1555–1569. https://doi.org/10.1099/mic.0.2008/018523-0
9. Cheng Y-Q, Tang G-L, Shen B (2003) Type I polyketide synthase requiring a discrete acyltransferase for polyketide biosynthesis. Proc Natl Acad Sci 100:3149–3154. https://doi.org/10.1073/pnas.0537286100
10. Du D, Katsuyama Y, Onaka H, Fujie M, Satoh N, Shin-ya K, Ohnishi Y (2016) Production of a novel amide-containing polyene by activating a cryptic biosynthetic gene cluster in Streptomyces sp. MSC090213JE08. ChemBioChem. https://doi.org/10.1002/cbic.201600167
11. Fischbach MA, Walsh CT (2006) Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic machinery, and mechanisms. Chem Rev 106:3468–3496. https://doi.org/10.1021/cr0503097
12. Gomez-Escribano JP, Song L, Fox DJ, Yeo V, Bibb MJ, Challis GL (2012) Structure and biosynthesis of the unusual polyketide alkaloid coelimycin P1, a metabolic product of the cpk gene cluster of Streptomyces coelicolor M145. Chem Sci 3:2716. https://doi.org/10.1039/c2sc20410j
13. Gottelt M, Kol S, Gomez-Escribano JP, Bibb M, Takano E (2010) Deletion of a regulatory gene within the cpk gene cluster reveals novel antibacterial activity in Streptomyces coelicolor A3(2). Microbiology 156:2343–2353. https://doi.org/10.1099/mic.0.038281-0
14. Gu L, Geders TW, Wang B, Gerwick WH, Hakansson K, Smith JL, Sherman DH (2007) GNAT-Like strategy for polyketide chain initiation. Science 318:970–974. https://doi.org/10.1126/science.1148790
15. Hashimoto K, Nihira T, Sakuda S, Yamada Y (1992) IM-2, a butyrolactone autoregulator, induces production of several nucleoside antibiotics in Streptomyces sp. FRI-5. J Ferment Bioeng 73:449–455. https://doi.org/10.1016/0922-338X(92)90136-I
16. He M, Varoglu M, Sherman DH (2000) Structural modeling and site-directed mutagenesis of the actinorhodin beta-ketoacyl-acyl carrier protein synthase. J Bacteriol 182:2619–2623
17. Helfrich EJN, Piel J (2016) Biosynthesis of polyketides by trans-AT polyketide synthases. Nat Prod Rep 33:231–316. https://doi.org/10.1039/b816430b
18. Huang W, Kim SJ, Liu J, Zhang W (2015) Identification of the polyketide biosynthetic machinery for the indolizidine alkaloid cyclizidine. Org Lett 17:5344–5347. https://doi.org/10.1021/acs.orglett.5b02707
19. Ikeda H, Nonomiya T, Usami M, Ohta T, Omura S (1999) Organization of the biosynthetic gene cluster for the polyketide anthelmintic macrolide avermectin in Streptomyces avermitilis. Proc Natl Acad Sci USA 96:9509–9514. https://doi.org/10.1073/pnas.96.17.9509
20. Ikeda H, Shin-Ya K, Omura S (2014) Genome mining of the Streptomyces avermitilis genome and development of genome-minimized hosts for heterologous expression of biosynthetic gene clusters. J Ind Microbiol Biotechnol 41:233–250. https://doi.org/10.1007/s10295-013-1327-x
21. Keatinge-Clay AT (2007) A tylosin ketoreductase reveals how chirality is determined in polyketides. Chem Biol 14:898–908. https://doi.org/10.1016/j.chembiol.2007.07.009
22. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics. John Innes Foundation, Norwich
23. Kitani S, Ikeda H, Sakamoto T, Nogochi S, Takuya N (2009) Characterization of a regulatory gene, aveR, for the biosynthesis of avermectin in Streptomyces avermitilis. Appl Microbiol Biotechnol 82:1089–1096. https://doi.org/10.1007/s00253-008-1850-2
24. Kitani S, Yamada Y, Nihira T (2001) Gene replacement analysis of the butyrolactone autoregulator receptor (FarA) reveals that FarA acts as a novel regulator in secondary metabolism of Streptomyces lavendulae FRI-5. J Bacteriol 183:4357–4363. https://doi.org/10.1128/JB.183.14.4357-4363.2001
25. Koehn FE, Carter GT (2005) The evolving role of natural products in drug discovery. Nat Rev Drug Discov 4:206–220. https://doi.org/10.1038/nrd1657
26. Komatsu M, Komatsu K, Koiwai H et al (2013) Engineered Streptomyces avermitilis host for heterologous expression of biosynthetic gene cluster for secondary metabolites. ACS Synth Biol 2:384–396. https://doi.org/10.1021/sb3001003
27. Komatsu M, Tsuda M, Omura S, Oikawa H, Ikeda H (2008) Identification and functional analysis of genes controlling biosynthesis of 2-methylisoborneol. Proc Natl Acad Sci USA 105:7422–7427. https://doi.org/10.1073/pnas.0802312105
28. Komatsu M, Uchiyama T, Omura S, Cane DE, Ikeda H (2010) Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism. Proc Natl Acad Sci USA 107:2646–2651. https://doi.org/10.1073/pnas.0914833107
29. Laureti L, Song L, Huang S, Corre C, Leblond P, Challis GL, Aigle B (2011) Identification of a bioactive 51-membered macrolide complex by activation of a silent polyketide synthase in Streptomyces ambofaciens. Proc Natl Acad Sci USA 108:6258–6263. https://doi.org/10.1073/pnas.1019077108
30. Mizutani S, Odai H, Masuda T et al (1989) Biological activities of IC201 ((3S,8E)-1,3-dihydroxy-8-decen-5-one), a low molecular weight immunomodulator produced by Streptomyces. J Antibiot (Tokyo) 42:952–959. https://doi.org/10.7164/antibiotics.42.952
31. Newman DJ, Cragg GM (2016) Natural products as sources of new drugs from 1981 to 2014. J Nat Prod 79:629–661. https://doi.org/10.1021/acs.jnatprod.5b01055
32. Ochi K, Hosaka T (2013) New strategies for drug discovery: activation of silent or weakly expressed microbial gene clusters. Appl Microbiol Biotechnol 97:87–98. https://doi.org/10.1007/s00253-012-4551-9
33. Ohnishi Y, Ishikawa J, Hara H et al (2008) Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J Bacteriol 190:4050–4060. https://doi.org/10.1128/JB.00204-08
34. Ohtsubo Y, Ikeda-Ohtsubo W, Nagata Y, Tsuda M (2008) GenomeMatcher: a graphical user interface for DNA sequence comparison. BMC Bioinf 9:376. https://doi.org/10.1186/1471-2105-9-376
35. Omura S (2011) Microbial metabolites: 45 years of wandering, wondering and discovering. Tetrahedron 67:6420–6459. https://doi.org/10.1016/j.tet.2011.03.117
36. Onaka H, Ozaki T, Mori Y, Izawa M, Hayashi S, Asamizu S (2015) Mycolic acid-containing bacteria activate heterologous secondary metabolite expression in Streptomyces lividans. J Antibiot (Tokyo) 68:1–4. https://doi.org/10.1038/ja.2015.31
37. Pait IGU, Kitani S, Kurniawan YN, Asa M, Iwai T, Ikeda H, Nihira T (2017) Identification and characterization of lbpA, an indigoidine biosynthetic gene in the γ-butyrolactone signaling system of Streptomyces lavendulae FRI-5. J Biosci Bioeng. https://doi.org/10.1016/j.jbiosc.2017.04.020
38. Reen FJ, Romano S, Dobson ADW, O’Gara F (2015) The sound of silence: activating silent biosynthetic gene clusters in marine microorganisms. Mar Drugs 13:4754–4783. https://doi.org/10.3390/md13084754
39. Reid R, Piagentini M, Rodriguez E et al (2003) A model of structure and catalysis for ketoreductase domains in modular polyketide synthases. Biochemistry 42:72–79. https://doi.org/10.1021/bi0268706
40. Scherlach K, Hertweck C (2009) Triggering cryptic natural product biosynthesis in microorganisms. Org Biomol Chem 7:1753. https://doi.org/10.1039/b821578b
41. Skiba MA, Sikkema AP, Fiers WD, Gerwick WH, Sherman DH, Aldrich CC, Smith JL (2016) Domain organization and active site architecture of a polyketide synthase C -methyltransferase. ACS Chem Biol 11:3319–3327. https://doi.org/10.1021/acschembio.6b00759
42. Staunton J, Weissman KJ (2001) Polyketide biosynthesis: a millennium review. Nat Prod Rep 18:380–416. https://doi.org/10.1039/a909079g
43. T and comparison to the other completely sequenced Pseudonocardiaceae. BMC Genom 13:465. https://doi.org/10.1186/1471-2164-13-465
44. Tanaka Y, Kasahara K, Hirose Y, Murakami K, Kugyama R, Ochi K (2013) Activation and products of the cryptic secondary metabolite biosynthetic gene clusters by rifampin resistance (rpoB) mutations in actinomycetes. J Bacteriol 195:2959–2970. https://doi.org/10.1128/JB.00147-13
45. Tanaka Y, Tokuyama S, Ochi K (2009) Activation of secondary metabolite-biosynthetic gene clusters by generating rsmG mutations in Streptomyces griseus. J Antibiot (Tokyo) 62:669–673. https://doi.org/10.1038/ja.2009.97
46. Tarazona G, Schleissner C, Rodríguez P, Pérez M, Cañedo LM, Cuevas C (2017) Streptenols F–I isolated from the marine-derived Streptomyces misionensis BAT-10-03-023. J Nat Prod. https://doi.org/10.1021/acs.jnatprod.6b01057
47. Traxler MF, Watrous JD, Alexandrov T, Dorrestein PC, Kolter R (2013) Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. MBio. https://doi.org/10.1128/mBio.00459-13
48. Wesener SR, Potharla VY, Cheng YQ (2011) Reconstitution of the FK228 biosynthetic pathway reveals cross talk between modular polyketide synthases and fatty acid synthase. Appl Environ Microbiol 77:1501–1507. https://doi.org/10.1128/AEM.01513-10
49. Wu J, Zaleski TJ, Valenzano C, Khosla C, Cane DE (2005) Polyketide double bond biosynthesis. Mechanistic analysis of the dehydratase-containing module 2 of the picromycin/methymycin polyketide synthase. J Am Chem Soc 127:17393–17404. https://doi.org/10.1021/ja055672+
50. Yamada Y, Arima S, Nagamitsu T et al (2015) Novel terpenes generated by heterologous expression of bacterial terpene synthase genes in an engineered Streptomyces host. J Antibiot (Tokyo) 68:1–10. https://doi.org/10.1038/ja.2014.171
51. Yamada Y, Kuzuyama T, Komatsu M, Shin-ya K, Omura S, Cane DE, Ikeda H (2015) Terpene synthases are widely distributed in bacteria. Proc Natl Acad Sci 112:857–862. https://doi.org/10.1073/pnas.1422108112
52. Yanai K, Murakami T, Bibb M (2006) Amplification of the entire kanamycin biosynthetic gene cluster during empirical strain improvement of Streptomyces kanamyceticus. Proc Natl Acad Sci USA 103:9661–9666. https://doi.org/10.1073/pnas.0603251103
53. Ye S, Molloy B, Braña AF et al (2017) Identification by genome mining of a type I polyketide gene cluster from Streptomyces argillaceus involved in the biosynthesis of pyridine and piperidine alkaloids argimycins P. Front Microbiol 8:1–18. https://doi.org/10.3389/fmicb.2017.00194
54. Yu D, Xu F, Zhang S et al (2013) Characterization of a methyltransferase involved in herboxidiene biosynthesis. Bioorganic Med Chem Lett 23:5667–5670. https://doi.org/10.1016/j.bmcl.2013.08.023
55. Zarins-Tutt JS, Barberi TT, Gao H et al (2016) Prospecting for new bacterial metabolites: a glossary of approaches for inducing, activating and upregulating the biosynthesis of bacterial cryptic or silent natural products. Nat Prod Rep 33:54–72. https://doi.org/10.1039/C5NP00111K
56. Zhang W, Li S, Zhu Y et al (2014) Heronamides D-F, polyketide macrolactams from the deep-sea-derived Streptomyces sp. SCSIO 03032. J Nat Prod 77:388–391. https://doi.org/10.1021/np400665a