Recent advances in genome mining of secondary metabolites in Aspergillus terreus

Frontiers in Microbiology

Volumn 5, Issue DEC, 2014, Pages

  Guo, Chun Jun ^a   Wang, Clay C C ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Aspergillus terreus; Genome mining; Natural products; Secondary metabolites

Indexed keywords

ACETYLARANOTIN; ALDEHYDE; ANTIBIOTIC AGENT; ARYL ACID; ASPERFURANONE; ASPULVINONE; ASTERRIQUINONE; ASZONALENIN; BENZODIAZEPINE; BRUTON TYROSINE KINASE; BUTYROLACTONE; FURANONE DERIVATIVE; ISOFLAVIPUCINE; MEVINOLIN; MYCOTOXIN; NANDROLONE PHENPROPIONATE; NONRIBOSOMAL PEPTIDE SYNTHETASE; POLYCYCLIC AROMATIC HYDROCARBON DERIVATIVE; POLYKETIDE; POLYKETIDE SYNTHASE; QUINONE DERIVATIVE; TERREIC ACID; TERREIN; TERRETONIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ALKYLATION; AROMATIZATION; ASPERGILLUS TERREUS; BIOINFORMATICS; BIOSYNTHESIS; COVALENT BOND; CYCLIZATION; CYTOTOXICITY; DEGRADATION; EPOXIDATION; GENE CLUSTER; GENE DELETION; GENETIC SCREENING; GENOMICS; HERBICIDAL ACTIVITY; HYDROXYLATION; METABOLITE; METHYLATION; NONHUMAN; OXIDATION; PLASTICITY; POLYMERIZATION; REDUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SECONDARY METABOLITE; TRANSAMINATION;

ASPERGILLUS TERREUS; FUNGI;

EID: 84920688369     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00717     Document Type: Review

References (58)

1. Arai, K., Rawlings, B. J., Yoshizawa, Y., and Vederas, J. C. (1989). Biosyntheses of antibiotic A26771B by Penicillium turbatum and dehydrocurvularin by Alternaria cinerariae: comparison of stereochemistry of polyketide and fatty acid enoyl thiol ester reductases. J. Am. Chem. Soc. 111, 3391-3399. doi: 10.1021/ja00191a042
2. Awakawa, T., Yokota, K., Funa, N., Doi, F., Mori, N., Watanabe, H., et al. (2009). Physically discrete beta-lactamase-type thioesterase catalyzes product release in atrochrysone synthesis by iterative type I polyketide synthase. Chem. Biol. 16, 613-623. doi: 10.1016/j.chembiol.2009.04.004
3. Balibar, C. J., Howard-Jones, A. R., and Walsh, C. T. (2007). Terrequinone A biosynthesis through L-tryptophan oxidation, dimerization and bisprenylation. Nat. Chem. Biol. 3, 584-592. doi: 10.1038/nchembio.2007.20
4. Birch, A. J., Cassera, A., and Jones, A. R. (1965). The biosynthesis of terrain. Chem. Commun. 167-168. doi: 10.1039/c19650000167
5. Boente, M. I. P., Kirby, G. W., and Robins, D. J. (1981). Biosynthetic incorporation of cyclo-(L-phenylalanyl-L-phenylalanyl) into bisdethiobis(methylthio)acetylaranotin in Aspergillus terreus. Chem. Commun. 619. doi: 10.1039/c39810000619
6. Boruta, T., and Bizukojc, M. (2014). Culture-based and sequence-based insights into biosynthesis of secondary metabolites by Aspergillus terreus ATCC 20542. J. Biotechnol. 175, 53-62. doi: 10.1016/j.jbiotec.2014.01.038
7. Brown, D. W., Yu, J. H., Kelkar, H. S., Fernandes, M., Nesbitt, T. C., Keller, N. P., et al. (1996). Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proc. Natl. Acad. Sci. U.S.A. 93, 1418-1422. doi: 10.1073/pnas.93.4.1418
8. Campbell, C. D., and Vederas, J. C. (2010). Biosynthesis of lovastatin and related metabolites formed by fungal iterative PKS enzymes. Biopolymers 93, 755-763. doi: 10.1002/bip.21428
9. Chiang, Y. M., Oakley, B. R., Keller, N. P., and Wang, C. C. (2010). Unraveling polyketide synthesis in members of the genus Aspergillus. Appl. Microbiol. Biotechnol. 86, 1719-1736. doi: 10.1007/s00253-010-2525-3
10. Chiang, Y. M., Oakley, C. E., Ahuja, M., Entwistle, R., Schultz, A., Chang, S. L., et al. (2013). An efficient system for heterologous expression of secondary metabolite genes in Aspergillus nidulans. J. Am. Chem. Soc. 135, 7720-7731. doi: 10.1021/ja401945a
11. Chiang, Y. M., Szewczyk, E., Davidson, A. D., Keller, N., Oakley, B. R., and Wang, C. C. (2009). A gene cluster containing two fungal polyketide synthases encodes the biosynthetic pathway for a polyketide, asperfuranone, in Aspergillus nidulans. J. Am. Chem. Soc. 131, 2965-2970. doi: 10.1021/ja8088185
12. Chooi, Y. H., and Tang, Y. (2012). Navigating the fungal polyketide chemical space: from genes to molecules. J. Org. Chem. 77, 9933-9953. doi: 10.1021/jo301592k
13. Cox, R. J. (2007). Polyketides, proteins and genes in fungi: programmed nano-machines begin to reveal their secrets. Org. Biomol. Chem. 5, 2010-2026. doi: 10.1039/b704420h
14. Davis, C., Carberry, S., Schrettl, M., Singh, I., Stephens, J. C., Barry, S. M., et al. (2011). The role of glutathione S-transferase GliG in gliotoxin biosynthesis in Aspergillus fumigatus. Chem. Biol. 18, 542-552. doi: 10.1016/j.chembiol.2010.12.022
15. Dolan, S. K., Owens, R. A., O'keeffe, G., Hammel, S., Fitzpatrick, D. A., Jones, G. W., et al. (2014). Regulation of nonribosomal peptide synthesis: bis-thiomethylation attenuates gliotoxin biosynthesis in Aspergillus fumigatus. Chem. Biol. 21, 999-1012. doi: 10.1016/j.chembiol.2014.07.006
16. Fujii, I., Ono, Y., Tada, H., Gomi, K., Ebizuka, Y., and Sankawa, U. (1996). Cloning of the polyketide synthase gene atX from Aspergillus terreus and its identification as the 6-methylsalicylic acid synthase gene by heterologous expression. Mol. Gen. Genet. 253, 1-10. doi: 10.1007/s004380050289
17. Gallagher, L., Owens, R. A., Dolan, S. K., O'keeffe, G., Schrettl, M., Kavanagh, K., et al. (2012). The Aspergillus fumigatus protein GliK protects against oxidative stress and is essential for gliotoxin biosynthesis. Eukaryot. Cell 11, 1226-1238. doi: 10.1128/EC.00113-12
18. Gressler, M., Zaehle, C., Scherlach, K., Hertweck, C., and Brock, M. (2011). Multifactorial induction of an orphan PKS-NRPS gene cluster in Aspergillus terreus. Chem. Biol. 18, 198-209. doi: 10.1016/j.chembiol.2010.12.011
19. Guo, C.-J., Knox, B. P., Chiang, Y.-M., Lo, H.-C., Sanchez, J. F., Lee, K.-H., et al. (2012). Molecular genetic characterization of a cluster in A. terreus for biosynthesis of the meroterpenoid terretonin. Org. Lett. 14, 5684-5687. doi: 10.1021/ol302682z
20. Guo, C. J., Knox, B. P., Sanchez, J. F., Chiang, Y. M., Bruno, K. S., and Wang, C. C. (2013a). Application of an efficient gene targeting system linking secondary metabolites to their biosynthetic genes in Aspergillus terreus. Org. Lett. 15, 3562-3565. doi: 10.1021/ol401384v
21. Guo, C.-J., Sun, W.-W., Bruno, K. S., and Wang, C. C. C. (2014). Molecular genetic characterization of terreic acid pathway in Aspergillus terreus. Org. Lett. 16, 5250-5253. doi: 10.1021/ol502242a
22. Guo, C. J., Yeh, H. H., Chiang, Y. M., Sanchez, J. F., Chang, S. L., Bruno, K. S., et al. (2013b). Biosynthetic pathway for the epipolythiodioxopiperazine acetylaranotin in Aspergillus terreus revealed by genome-based deletion analysis. J. Am. Chem. Soc. 135, 7205-7213. doi: 10.1021/ja3123653
23. Hill, A. M. (2006). The biosynthesis, molecular genetics and enzymology of the polyketide-derived metabolites. Nat. Prod. Rep. 23, 256-320. doi: 10.1039/b301028g
24. Hill, R. A., Carter, R. H., and Staunton, J. (1981). Biosynthesis of fungal metabolites. Terrein, a metabolite of Aspergillus terreus Thom. J. Chem. Soc. Perkin Trans. 1, 2570-2576. doi: 10.1039/p19810002570
25. Itoh, T., Tokunaga, K., Radhakrishnan, E. K., Fujii, I., Abe, I., Ebizuka, Y., et al. (2012). Identification of a key prenyltransferase involved in biosynthesis of the most abundant fungal meroterpenoids derived from 3,5-dimethylorsellinic acid. Chembiochem 13, 1132-1135. doi: 10.1002/cbic.201200124
26. Jimenez-Oses, G., Osuna, S., Gao, X., Sawaya, M. R., Gilson, L., Collier, S. J., et al. (2014). The role of distant mutations and allosteric regulation on LovD active site dynamics. Nat. Chem. Biol. 10, 431-436. doi: 10.1038/nchembio.1503
27. Kawakami, Y., Hartman, S. E., Kinoshita, E., Suzuki, H., Kitaura, J., Yao, L., et al. (1999). Terreic acid, a quinone epoxide inhibitor of Bruton's tyrosine kinase. Proc. Natl. Acad. Sci. U.S.A. 96, 2227-2232. doi: 10.1073/pnas.96.5.2227
28. Keller, N. P., Turner, G., and Bennett, J. W. (2005). Fungal secondary metabolism - from biochemistry to genomics. Nat. Rev. Microbiol. 3, 937-947. doi: 10.1038/nrmicro1286
29. Khaldi, N., Seifuddin, F. T., Turner, G., Haft, D., Nierman, W. C., Wolfe, K. H., et al. (2010). SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet. Biol. 47, 736-741. doi: 10.1016/j.fgb.2010.06.003
30. Kiriyama, N., Nitta, K., Sakaguchi, Y., Taguchi, Y., and Yamamoto, Y. (1977). Studies on the metabolic products of Aspergillus terreus. III. Metabolites of the strain IFO 8835. Chem. Pharm. Bull. 25, 2593-2601. doi: 10.1248/cpb.25.2593
31. Kuck, U., and Hoff, B. (2010). New tools for the genetic manipulation of filamentous fungi. Appl. Microbiol. Biotechnol. 86, 51-62. doi: 10.1007/s00253-009-2416-7
32. Matsuda, Y., Awakawa, T., Itoh, T., Wakimoto, T., Kushiro, T., Fujii, I., et al. (2012). Terretonin biosynthesis requires methylation as essential step for cyclization. Chembiochem 13, 1738-1741. doi: 10.1002/cbic.201200369
33. McIntyre, C. R., Scott, F. E., Simpson, T. J., Trimble, L. A., and Vederas, J. C. (1989). Application of stable isotope labelling methodology to the biosynthesis of the mycotoxin, terretonin, by Aspergillus terreus: incorporation of 13C-labelled acetates and methionine, 2H- and 13C, 18O-labelled ethyl 3,5-dimethylorsellinate and oxygen-18 gas. Tetrahedron 45, 2307-2321. doi: 10.1016/S0040-4020(01)83433-5
34. McIntyre, C. R., Simpson, T. J., Stenzel, D. J., Bartlett, A. J., Q'brien, E., and Holker, J. S. E. (1982). Biosynthesis of the meroterpenoid metabolites, austin and terretonin: incorporation of 3,5-dimethylorsellinate. Chem. Commun. 781. doi: 10.1039/c39820000781
35. Nayak, T., Szewczyk, E., Oakley, C. E., Osmani, A., Ukil, L., Murray, S. L., et al. (2006). A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172, 1557-1566. doi: 10.1534/genetics.105.052563
36. Nitta, K., Fujita, N., Yoshimura, T., Arai, K., and Yamamoto, Y. (1983). Metabolic products of Aspergillus terreus. IX. Biosynthesis of butyrolactone derivatives isolated from strains IFO 8835 and 4100. Chem. Pharm. Bull. 31, 1528-1533. doi: 10.1248/cpb.31.1528
37. Patron, N. J., Waller, R. F., Cozijnsen, A. J., Straney, D. C., Gardiner, D. M., Nierman, W. C., et al. (2007). Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evol. Biol. 7:174. doi: 10.1186/1471-2148-7-174
38. Proctor, R. H., Brown, D. W., Plattner, R. D., and Desjardins, A. E. (2003). Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet. Biol. 38, 237-249. doi: 10.1016/S1087-1845(02)00525-X
39. Read, G., and Vining, L. C. (1968). The biosynthesis of terreic acid. Chem. Commun. 935. doi: 10.1039/c19680000935
40. Read, G., Westlake, D. W., and Vining, L. C. (1969). Quinone epoxides. V. The biosynthesis of terreic acid. Can. J. Biochem. 47, 1071-1079. doi: 10.1139/o69-171
41. Sanchez, J. F., Somoza, A. D., Keller, N. P., and Wang, C. C. C. (2012). Advances in Aspergillus secondary metabolite research in the post-genomic era. Nat. Prod. Rep. 29, 351. doi: 10.1039/c2np00084a
42. Scharf, D. H., Chankhamjon, P., Scherlach, K., Heinekamp, T., Roth, M., Brakhage, A. A., et al. (2012). Epidithiol formation by an unprecedented twin carbon-sulfur lyase in the gliotoxin pathway. Angew. Chem. Int. Ed. Engl. 51, 10064-10068. doi: 10.1002/anie.201205041
43. Scharf, D. H., Chankhamjon, P., Scherlach, K., Heinekamp, T., Willing, K., Brakhage, A. A., et al. (2013). Epidithiodiketopiperazine biosynthesis: a four-enzyme cascade converts glutathione conjugates into transannular disulfide bridges. Angew. Chem. Int. Ed. Engl. 52, 11092-11095. doi: 10.1002/anie.201305059
44. Scharf, D. H., Habel, A., Heinekamp, T., Brakhage, A. A., and Hertweck, C. (2014). Opposed effects of enzymatic gliotoxin N- and S-methylations. J. Am. Chem. Soc. 136, 11674-11679. doi: 10.1021/ja5033106
45. Scharf, D. H., Heinekamp, T., Remme, N., Hortschansky, P., Brakhage, A. A., and Hertweck, C. (2011a). Biosynthesis and function of gliotoxin in Aspergillus fumigatus. Appl. Microbiol. Biotechnol. 93, 467-472. doi: 10.1007/s00253-011-3689-1
46. Scharf, D. H., Remme, N., Habel, A., Chankhamjon, P., Scherlach, K., Heinekamp, T., et al. (2011b). A dedicated glutathione S-transferase mediates carbon-sulfur bond formation in gliotoxin biosynthesis. J. Am. Chem. Soc. 133, 12322-12325. doi: 10.1021/ja201311d
47. Scharf, D. H., Remme, N., Heinekamp, T., Hortschansky, P., Brakhage, A. A., and Hertweck, C. (2010). Transannular disulfide formation in gliotoxin biosynthesis and its role in self-resistance of the human pathogen Aspergillus fumigatus. J. Am. Chem. Soc. 132, 10136-10141. doi: 10.1021/ja103262m
48. Schrettl, M., Carberry, S., Kavanagh, K., Haas, H., Jones, G. W., O'brien, J., et al. (2010). Self-protection against gliotoxin-a component of the gliotoxin biosynthetic cluster, GliT, completely protects Aspergillus fumigatus against exogenous gliotoxin. PLoS Pathog. 6:e1000952. doi: 10.1371/journal.ppat.1000952
49. Szewczyk, E., Nayak, T., Oakley, C. E., Edgerton, H., Xiong, Y., Taheri-Talesh, N., et al. (2006). Fusion PCR and gene targeting in Aspergillus nidulans. Nat. Protoc. 1, 3111-3120. doi: 10.1038/nprot.2006.405
50. Wang, M., Beissner, M., and Zhao, H. (2014). Aryl-aldehyde formation in fungal polyketides: discovery and characterization of a distinct biosynthetic mechanism. Chem. Biol. 21, 257-263. doi: 10.1016/j.chembiol.2013.12.005
51. Wang, M., and Zhao, H. (2014). Characterization and engineering of the adenylation domain of a NRPS-like protein: a potential biocatalyst for aldehyde generation. ACS Catal. 4, 1219-1225. doi: 10.1021/cs500039v
52. Xu, W., Chooi, Y.-H., Choi, J. W., Li, S., Vederas, J. C., Da Silva, N. A., et al. (2013a). LovG: The thioesterase required for dihydromonacolin L release and lovastatin nonaketide synthase turnover in lovastatin biosynthesis. Angew. Chem. Int. Ed. Engl. 52, 6472-6475. doi: 10.1002/anie.201302406
53. Xu, Y., Espinosa-Artiles, P., Schubert, V., Xu, Y. M., Zhang, W., Lin, M., et al. (2013b). Characterization of the biosynthetic genes for 10,11-dehydrocurvularin, a heat shock response-modulating anticancer fungal polyketide from Aspergillus terreus. Appl. Environ. Microbiol. 79, 2038-2047. doi: 10.1128/AEM.03334-12
54. Xu, Y., Zhou, T., Zhou, Z., Su, S., Roberts, S. A., Montfort, W. R., et al. (2013c). Rational reprogramming of fungal polyketide first-ring cyclization. Proc. Natl. Acad. Sci. U.S.A. 110, 5398-5403. doi: 10.1073/pnas.1301201110
55. Yamamoto, H., Moriyama, K., Jinnouchi, H., and Yagishita, K. (1980). Studies on terreic acid. Jpn. J. Antibiot. 33, 320-328. doi: 10.11553/antibiotics1968b.33.320
56. Yin, W. B., Grundmann, A., Cheng, J., and Li, S. M. (2009). Acetylaszonalenin biosynthesis in Neosartorya fischeri. Identification of the biosynthetic gene cluster by genomic mining and functional proof of the genes by biochemical investigation. J. Biol. Chem. 284, 100-109. doi: 10.1074/jbc.M807606200
57. Yu, J.-H., Hamari, Z., Han, K.-H., Seo, J.-A., Reyes-Domínguez, Y., and Scazzocchio, C. (2004). Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet. Biol. 41, 973-981. doi: 10.1016/j.fgb.2004.08.001
58. Zaehle, C., Gressler, M., Shelest, E., Geib, E., Hertweck, C., and Brock, M. (2014). Terrein biosynthesis in Aspergillus terreus and its impact on phytotoxicity. Chem. Biol. 21, 719-731. doi: 10.1016/j.chembiol.2014.03.010