Genome Mining of Alkaloidal Terpenoids from a Hybrid Terpene and Nonribosomal Peptide Biosynthetic Pathway

Journal of the American Chemical Society

Volumn 142, Issue 2, 2020, Pages 710-714

  Yee, Danielle A ^a   Kakule, Thomas B ^a   Cheng, Wei ^a,c   Chen, Mengbin ^a   Chong, Christine T Y ^b   Hai, Yang ^a   Hang, Leibniz F ^b   Hung, Yiu Sun ^a   Liu, Nicholas ^a   Ohashi, Masao ^a   Okorafor, Ikechukwu C ^a   Song, Yongxiang ^a   Tang, Mancheng ^a   Zhang, Zhuan ^a   Tang, Yi ^a,b  

^a Department of Civil and Environmental Engineering   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; ENZYMES; GENES; LIPIDS; METABOLITES; PEPTIDES;

BIOSYNTHETIC PATHWAY; GENOME MINING; HETEROLOGOUS EXPRESSION; METABOLITE ANALYSIS; NATURAL PRODUCTS; NONRIBOSOMAL PEPTIDE; NONRIBOSOMAL PEPTIDE SYNTHETASES; SESQUITERPENES;

TERPENES;

5,5 DIMETHYL PIPECOLATE; CADAVERINE; DIMETHYLCADAVERINE; FLAVUNOIDINE; FUNGAL ENZYME; NONRIBOSOMAL PEPTIDE SYNTHETASE; PIPECOLIC ACID; SESQUITERPENE; TERPENE CYCLASE; TERPENOID DERIVATIVE; UNCLASSIFIED DRUG; ALKALOID; PEPTIDE; TERPENE;

ACYLATION; ARTICLE; ASPERGILLUS NIDULANS; BIOSYNTHESIS; CARBON NITROGEN BOND; CHEMICAL STRUCTURE; COVALENT BOND; CRYSTAL STRUCTURE; FLV GENE; FUNGAL GENE; GENE CLUSTER; GENOME ANALYSIS; GENOME MINING; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; METABOLITE; NONHUMAN; PEPTIDE SYNTHESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; CHEMISTRY; GENOME; RIBOSOME;

ALKALOIDS; GENOME; PEPTIDES; RIBOSOMES; TERPENES;

EID: 85077935102     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/jacs.9b13046     Document Type: Article

References (48)

1. Lin, C. I.; McCarty, R. M.; Liu, H. W. The enzymology of organic transformations: a survey of name reactions in biological systems. Angew. Chem., Int. Ed. 2017, 56, 3446-3489, 10.1002/anie.201603291
2. Rix, U.; Fischer, C.; Remsing, L. L.; Rohr, J. Modification of post-PKS tailoring steps through combinatorial biosynthesis. Nat. Prod. Rep. 2002, 19, 542-580, 10.1039/b103920m
3. Olano, C.; Méndez, C.; Salas, J. A. Post-PKS tailoring steps in natural product-producing actinomycetes from the perspective of combinatorial biosynthesis. Nat. Prod. Rep. 2010, 27, 571-616, 10.1039/b911956f
4. Tang, M. C.; Zou, Y.; Watanabe, K.; Walsh, C. T.; Tang, Y. Oxidative cyclization in natural product biosynthesis. Chem. Rev. 2017, 117, 5226-5333, 10.1021/acs.chemrev.6b00478
5. Cochrane, R. V.; Vederas, J. C. Highly selective but multifunctional oxygenases in secondary metabolism. Acc. Chem. Res. 2014, 47, 3148-3161, 10.1021/ar500242c
6. Cox, R. Oxidative rearrangements during fungal biosynthesis. Nat. Prod. Rep. 2014, 31, 1405-1424, 10.1039/C4NP00059E
7. Cox, R. J. Polyketides, proteins and genes in fungi: programmed nano-machines begin to reveal their secrets. Org. Biomol. Chem. 2007, 5, 2010-2026, 10.1039/b704420h
8. Sato, M.; Dander, J. E.; Sato, C.; Hung, Y. S.; Gao, S. S.; Tang, M. C.; Hang, L.; Winter, J. M.; Garg, N. K.; Watanabe, K.; Tang, Y. Collaborative biosynthesis of maleimide-and succinimide-containing natural products by fungal polyketide megasynthases. J. Am. Chem. Soc. 2017, 139, 5317-5320, 10.1021/jacs.7b02432
9. Boettger, D.; Hertweck, C. Molecular diversity sculpted by fungal PKS-NRPS hybrids. ChemBioChem 2013, 14, 28-42, 10.1002/cbic.201200624
10. Itoh, T.; Tokunaga, K.; Matsuda, Y.; Fujii, I.; Abe, I.; Ebizuka, Y.; Kushiro, T. Reconstitution of a fungal meroterpenoid biosynthesis reveals the involvement of a novel family of terpene cyclases. Nat. Chem. 2010, 2, 858-864, 10.1038/nchem.764
11. Matsuda, Y.; Abe, I. Biosynthesis of fungal meroterpenoids. Nat. Prod. Rep. 2016, 33, 26-53, 10.1039/C5NP00090D
12. Lin, H. C.; Chooi, Y. H.; Dhingra, S.; Xu, W.; Calvo, A. M.; Tang, Y. The fumagillin biosynthetic gene cluster in Aspergillus fumigatus encodes a cryptic terpene cyclase involved in the formation of β-trans-bergamotene. J. Am. Chem. Soc. 2013, 135, 4616-4619, 10.1021/ja312503y
13. Schor, R.; Schotte, C.; Wibberg, D.; Kalinowski, J.; Cox, R. J. Three previously unrecognised classes of biosynthetic enzymes revealed during the production of xenovulene A. Nat. Commun. 2018, 9, 1963, 10.1038/s41467-018-04364-9
14. Li, S. M. Prenylated indole derivatives from fungi: structure diversity, biological activities, biosynthesis and chemoenzymatic synthesis. Nat. Prod. Rep. 2010, 27, 57-78, 10.1039/B909987P
15. Ding, Y.; Wet, J. R. d.; Cavalcoli, J.; Li, S.; Greshock, T. J.; Miller, K. A.; Finefield, J. M.; Sunderhaus, J. D.; McAfoos, T. J.; Tsukamoto, S.; Williams, R. M.; Sherman, D. H. Genome-based characterization of two prenylation steps in the assembly of the stephacidin and notoamide anticancer agents in a marine-derived Aspergillus sp. J. Am. Chem. Soc. 2010, 132, 12733-12740, 10.1021/ja1049302
16. Grundmann, A.; Kuznetsova, T.; Afiyatullov, S. S.; Li, S. M. FtmPT2, an N-Prenyltransferase from Aspergillus fumigatus, Catalyses the Last Step in the Biosynthesis of Fumitremorgin B. ChemBioChem 2008, 9, 2059-2063, 10.1002/cbic.200800240
17. Augustiniak, H.; Forche, E.; Reichenbach, H.; Wray, V.; Graefe, U.; Hoefle, G. Isolation and structure elucidation of ergokonin A and B; two new antifungal sterol antibiotics from Trichoderma koningii. Liebigs Ann. Chem. 1991, 4, 361-366, 10.1002/jlac.199119910163
18. Cóbar, O. M. Survey of 2, 11-cyclized cembranoids from Caribbean sources. Nat. Prod. Res. 2009, 23, 26-43, 10.1080/14786410701760797
19. Lee, C. F.; Chen, L. X.; Chiang, C. Y.; Lai, C. Y.; Lin, H. C. Biosynthesis of Norsesquiterpene Aculenes Requires Three Cytochrome P450s to Catalyze a Stepwise Demethylation Process. Angew. Chem., Int. Ed. 2019, 58, 18414-18418, 10.1002/anie.201910200
20. Rynkiewicz, M. J.; Cane, D. E.; Christianson, D. W. Structure of trichodiene synthase from Fusarium sporotrichioides provides mechanistic inferences on the terpene cyclization cascade. Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 13543-13548, 10.1073/pnas.231313098
21. Chiba, R.; Minami, A.; Gomi, K.; Oikawa, H. Identification of ophiobolin F synthase by a genome mining approach: a sesterterpene synthase from Aspergillus clavatus. Org. Lett. 2013, 15, 594-597, 10.1021/ol303408a
22. Nagasawa, T.; Kanzaki, H.; Yamada, H. Cystathionine gamma-lyase of Streptomyces phaeochromogenes. The occurrence of cystathionine gamma-lyase in filamentous bacteria and its purification and characterization. J. Biol. Chem. 1984, 259, 10393-10403
23. Wei, Y.; Perez, L. J.; Ng, W. L.; Semmelhack, M. F.; Bassler, B. L. Mechanism of Vibrio cholerae autoinducer-1 biosynthesis. ACS Chem. Biol. 2011, 6, 356-365, 10.1021/cb1003652
24. Liang, J.; Han, Q.; Tan, Y.; Ding, H.; Li, J. Current Advances on Structure-Function Relationships of Pyridoxal 5′ Phosphate-Dependent Enzymes. Front. Mol. Biosci. 2019, 6, 4, 10.3389/fmolb.2019.00004
25. Gao, S. S.; Naowarojna, N.; Cheng, R.; Liu, X.; Liu, P. Recent examples of α-ketoglutarate-dependent mononuclear non-haem iron enzymes in natural product biosyntheses. Nat. Prod. Rep. 2018, 35, 792-837, 10.1039/C7NP00067G
26. Herr, C. Q.; Hausinger, R. P. Amazing diversity in biochemical roles of Fe (II)/2-oxoglutarate oxygenases. Trends Biochem. Sci. 2018, 43, 517-532, 10.1016/j.tibs.2018.04.002
27. Islam, M. S.; Leissing, T. M.; Chowdhury, R.; Hopkinson, R. J.; Schofield, C. J. 2-Oxoglutarate-dependent oxygenases. Annu. Rev. Biochem. 2018, 87, 585-620, 10.1146/annurev-biochem-061516-044724
28. Qian, C.; Zhou, M. M. SET domain protein lysine methyltransferases: Structure, specificity and catalysis. Cell. Mol. Life Sci. 2006, 63, 2755-2763, 10.1007/s00018-006-6274-5
29. Yanagisawa, M.; Sakal, A.; Adachi, K.; Sano, T.; Watanabe, K.; Tanaka, Y.; Okuda, T. Hispidospermidin, a novel phospholipase C inhibitor produced by Chaetosphaeronema hispidulum (Cda) Moesz NR 7127. J. Antibiot. 1994, 47, 1-5, 10.7164/antibiotics.47.1
30. Ohtsuka, T.; Itezono, Y.; Nakayama, N.; Sakai, A.; Shimma, N.; Yokose, K.; Seto, H. Hispidospermidin, a novel Phospholipase c inhibitor produced by Chaetosphaeronema hispidulum (Cda) Moesz NR 7127. J. Antibiot. 1994, 47, 6-15, 10.7164/antibiotics.47.6
31. Frontier, A. J.; Raghavan, S.; Danishefsky, S. J. Stereocontrolled Total Synthesis of Hispidospermidin. J. Am. Chem. Soc. 1997, 119, 6686-6687, 10.1021/ja970889s
32. Frontier, A. J.; Raghavan, S.; Danishefsky, S. J. A highly stereoselective total synthesis of hispidospermidin: derivation of a pharmacophore model. J. Am. Chem. Soc. 2000, 122, 6151-6159, 10.1021/ja9944960
33. Overman, L. E.; Tomasi, A. L. Enantioselective total synthesis of hispidospermidin. J. Am. Chem. Soc. 1998, 120, 4039-4040, 10.1021/ja974361z
34. Tamiya, J.; Sorensen, E. J. A Concise Synthesis of (-)-Hispidospermidin Guided by a Postulated Biogenesis. J. Am. Chem. Soc. 2000, 122, 9556-9557, 10.1021/ja0026758
35. Tamiya, J.; Sorensen, E. J. A spontaneous bicyclization facilitates a synthesis of (-)-hispidospermidin. Tetrahedron 2003, 59, 6921-6932, 10.1016/S0040-4020(03)00936-0
36. Hartmann, M.; Kim, D.; Bernsdorff, F.; Ajami-Rashidi, Z.; Scholten, N.; Schreiber, S.; Zeier, T.; Schuck, S.; Reichel-Deland, V.; Zeier, J. Biochemical principles and functional aspects of pipecolic acid biosynthesis in plant immunity. Plant Physiol. 2017, 174, 124-153, 10.1104/pp.17.00222
37. Huang, J. L.; Tang, Y.; Yu, C. P.; Sanyal, D.; Jia, X.; Liu, X.; Guo, Y.; Chang, W. C. Mechanistic investigation of oxidative decarboxylation catalyzed by two iron (II)-and 2-oxoglutarate-dependent enzymes. Biochemistry 2018, 57, 1838-1841, 10.1021/acs.biochem.8b00115
38. Yu, C. P.; Tang, Y.; Cha, L.; Milikisiyants, S.; Smirnova, T. I.; Smirnov, A. I.; Guo, Y.; Chang, W. C. Elucidating the Reaction Pathway of Decarboxylation-Assisted Olefination Catalyzed by a Mononuclear Non-Heme Iron Enzyme. J. Am. Chem. Soc. 2018, 140, 15190-15193, 10.1021/jacs.8b10077
39. van der Donk, W. A.; Krebs, C.; Bollinger, J. M., Jr Substrate activation by iron superoxo intermediates. Curr. Opin. Struct. Biol. 2010, 20, 673-683, 10.1016/j.sbi.2010.08.005
40. Phelan, R. M.; Townsend, C. A. Mechanistic insights into the bifunctional non-heme iron oxygenase carbapenem synthase by active site saturation mutagenesis. J. Am. Chem. Soc. 2013, 135, 7496-7502, 10.1021/ja311078s
41. Harvey, C. J.; Tang, M.; Schlecht, U.; Horecka, J.; Fischer, C. R.; Lin, H. C.; Li, J.; Naughton, B.; Cherry, J.; Miranda, M.; Li, Y. F.; Chu, A. M.; Hennessy, J. R.; Vandova, G. A.; Inglis, D.; Aiyar, R. S.; Steinmetz, L. M.; Davis, R. W.; Medema, M. H.; Sattely, E.; Khosla, C.; St. Onge, R. P.; Tang, Y.; Hillenmeyer, M. E. HEx: a heterologous expression platform for the discovery of fungal natural products. Sci. Adv. 2018, 4, eaar5459 10.1126/sciadv.aar5459
42. Kurosawa, S.; Bando, M.; Mori, K. Synthesis of (1R, 4R, 5S)-(+)-Acoradiene, the Structure Proposed for the Aggregation Pheromone of the Broad-Horned Flour Beetle. Eur. J. Org. Chem. 2001, 2001, 4395-4399, 10.1002/1099-0690(200112)2001:23<4395::AID-EJOC4395>3.0.CO;2-Q
43. Tomita, B.; Hirose, Y. Allo-cedrol: a new tricarbocyclic sesquiterpene alcohol. Phytochemistry 1973, 12, 1409-1414, 10.1016/0031-9422(73)80575-8
44. Shuler, W. G.; Combee, L. A.; Falk, I. D.; Hilinski, M. K. Intermolecular Electrophilic Addition of Epoxides to Alkenes: [3+ 2] Cycloadditions Catalyzed by Lewis Acids. Eur. J. Org. Chem. 2016, 2016, 3335-3338, 10.1002/ejoc.201600651
45. McGee, T. P.; Skinner, H. B.; Bankaitis, V. A. Functional redundancy of CDP-ethanolamine and CDP-choline pathway enzymes in phospholipid biosynthesis: ethanolamine-dependent effects on steady-state membrane phospholipid composition in Saccharomyces cerevisiae. J. Bacteriol. 1994, 176, 6861-6868, 10.1128/jb.176.22.6861-6868.1994
46. Fillinger, S.; Ruijter, G.; Tamás, M. J.; Visser, J.; Thevelein, J. M.; D'enfert, C. Molecular and physiological characterization of the NAD-dependent glycerol 3-phosphate dehydrogenase in the filamentous fungus Aspergillus nidulans. Mol. Microbiol. 2001, 39, 145-157, 10.1046/j.1365-2958.2001.02223.x
47. Dijkema, C.; Rijcken, R. P.; Kester, H. C.; Visser, J. 13C-NMR studies on the influence of pH and nitrogen source on polyol pool formation in Aspergillus nidulans. FEMS Microbiol. Lett. 1986, 33, 125-131, 10.1111/j.1574-6968.1986.tb01225.x
48. Brunson, J. K.; McKinnie, S. M.; Chekan, J. R.; McCrow, J. P.; Miles, Z. D.; Bertrand, E. M.; Bielinski, V. A.; Luhavaya, H.; Oborník, M.; Smith, G. J.; Hutchins, D. A.; Allen, A. E.; Moore, B. S. Biosynthesis of the neurotoxin domoic acid in a bloom-forming diatom. Science 2018, 361, 1356-1358, 10.1126/science.aau0382