Culture-based and sequence-based insights into biosynthesis of secondary metabolites by Aspergillus terreus ATCC 20542

Journal of Biotechnology

Volumn 175, Issue 1, 2014, Pages 53-62

  Boruta, Tomasz ^a   Bizukojc, Marcin ^a  

^a LODZ UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

(+) Geodin; Aspergillus terreus; Citrinin; Lovastatin; Terreic acid

Indexed keywords

(+)-GEODIN; ASPERGILLUS TERREUS; CITRININ; LOVASTATIN; TERREIC ACID;

ASPERGILLUS; BIOCHEMISTRY; BIOSYNTHESIS; METABOLITES;

GENES;

ALPHA,BETA DEHYDROCURVULARIN; CITRININ; FUNGAL ENZYME; GEODIN; MEVINOLIN; MEVINOLINIC ACID; MONACOLIN L; TERREIC ACID; TERREIN; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS TERREUS; BIOCHEMISTRY; BIOSYNTHESIS; CULTURE MEDIUM; FUNGAL GENE; FUNGAL GENETICS; FUNGAL STRAIN; FUNGUS CULTURE; GENE CLUSTER; GENE LOCUS; GENE SEQUENCE; PRIORITY JOURNAL;

(+)-GEODIN; ASPERGILLUS TERREUS; CITRININ; LOVASTATIN; TERREIC ACID;

ASPERGILLUS; BENZOFURANS; CITRININ; CULTURE MEDIA; FUNGAL PROTEINS; GENES, FUNGAL; GENOME, FUNGAL; LOVASTATIN; MODELS, CHEMICAL; MULTIGENE FAMILY; QUINONES; SECONDARY METABOLISM; SEQUENCE ANALYSIS;

EID: 84896760851     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2014.01.038     Document Type: Article

References (62)

1. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
2. Artigot M.P., Loiseau N., Laffitte J., Mas-Reguieg L., Tadrist S., Oswald I.P., Puel O. Molecular cloning and functional characterization of two CYP619 cytochrome P450s involved in biosynthesis of patulin in Aspergillus clavatus. Microbiology 2009, 155:1738-1747.
3. Askenazi M., Driggers E.M., Holtzman D.A., Norman T.C., Iverson S., Zimmer D.P., Boers M.E., Blomquist P.R., Martinez E.J., Monreal A.W., Feibelman T.P., Mayorga M.E., Maxon M.E., Sykes K., Tobin J.V., Cordero E., Salama S.R., Trueheart J., Royer J.C., Madden K.T. Integrating transcriptional and metabolite profiles to direct the engineering of lovastatin-producing fungal strains. Nat. Biotechnol. 2003, 21:150-156.
4. Awakawa T., Yokota K., Funa N., Doi F., Mori N., Watanabe H., Horinouchi S. Physically discrete beta-lactamase-type thioesterase catalyzes product release in atrochrysone synthesis by iterative type I polyketide synthase. Chem. Biol. 2009, 16:613-623.
5. Balakrishnan B., Karki S., Chiu S.H., Kim H.J., Suh J.W., Nam B., Yoon Y.M., Chen C.C., Kwon H.J. Genetic localization and in vivo characterization of a Monascus azaphilone pigment biosynthetic gene cluster. Appl. Microbiol. Biotechnol. 2013, 97:6337-6345.
6. Barber J., Carter R.H., Garson M.J., Staunton J. The biosynthesis of citrinin by Penicillium citrinum. J. Chem. Soc. Perkin Trans. 1981, 1:2577-2583.
7. 2O. J. Chem. Soc. Chem. Commun. 1979, 1098-1099.
8. 2H nuclear magnetic resonance spectroscopy. J. Chem. Soc. Chem. Commun. 1980, 552-554.
9. Barber J., Staunton J. Citrinin biosynthesis in P. citrinum: incorporation of a deuterium-labelled advanced precursor in the presence of a specific inhibitor of an early step. J. Chem. Soc. Chem. Commun. 1980, 1163-1164.
10. Barber J., Staunton J. New insights into polyketide metabolism; the use of protium as a tracer in the biosynthesis of citrinin by Penicillium citrinum. J. Chem. Soc. Perkin Trans. 1980, 1:2244-2248.
11. Bennett J.W., Klich M. Mycotoxins. Clin. Microbiol. Rev. 2003, 16:497-516.
12. Bizukojc M., Pawlak M., Boruta T., Gonciarz J. Effect of pH on biosynthesis of lovastatin and other secondary metabolites by Aspergillus terreus ATCC 20542. J. Biotechnol. 2012, 162:253-261.
13. Bode H., Bethe B., Höfs R., Zeeck A. Big effects from small changes: possible ways to explore nature's chemical diversity. ChemBioChem 2002, 3:619-627.
14. Boruta T., Bizukojc M., Ledakowicz S. Bioinformatyczna analiza przewidywanego klastra genów biosyntezy (+)-geodyny u Aspergillus terreus. Inż. Ap. Chem. 2012, 51:92-94. (article in Polish).
15. Brakhage A.A. Regulation of fungal secondary metabolism. Nat. Rev. Microbiol. 2013, 11:21-32.
16. Brakhage A.A., Schroeckh V. Fungal secondary metabolites - strategies to activate silent gene clusters. Fungal Genet. Biol. 2011, 48:15-22.
17. Carter R.H., Garson M.J., Staunton J. Biosynthesis of citrinin: incorporation studies with advanced precursors. J. Chem. Soc. Chem. Commun. 1979, 1097-1098.
18. Casas Lopez J.L., Sanchez Perez J.A., Fernandez Sevilla J.M., Acien Fernandez F.G., Molina Grima E., Chisti Y. Production of lovastatin by Aspergillus terreus: effects of the C:N ratio and the principal nutrients on growth and metabolite production. Enzyme Microb. Technol. 2003, 33:270-277.
19. Chang P.K. The Aspergillus parasiticus protein AFLJ interacts with the aflatoxin pathway-specific regulator AFLR. Mol Genet. Genomics 2003, 268:711-719.
20. Chen Z.G., Fujii I., Ebizuka Y., Sankawa U. Emodin O-methyltransferase from Aspergillus terreus. Arch. Microbiol. 1992, 158:29-34.
21. Chen Z.G., Fujii I., Ebizuka Y., Sankawa U. Purification and characterization of emodinanthrone oxygenase from Aspergillus terreus. Phytochemistry 1995, 38:299-305.
22. Chen Y.P., Tseng C.P., Liaw L.L., Wang C.L., Chen I.C., Wu W.J., Wu M.D., Yuan G.F. Cloning and characterization of monacolin K biosynthetic gene cluster from Monascus pilosus. J. Agric. Food Chem. 2008, 56:5639-5646.
23. Chiang Y.M., Oakley B.R., Keller N.P., Wang C.C. Unraveling polyketide synthesis in members of the genus Aspergillus. Appl. Microbiol. Biotechnol. 2010, 86:1719-1736.
24. Chiang Y.M., Szewczyk E., Davidson A.D., Entwistle R., Keller N.P., Wang C.C., Oakley B.R. Characterization of the Aspergillus nidulans monodictyphenone gene cluster. Appl. Environ. Microbiol. 2010, 76:2067-2074.
25. Chiang Y.M., Szewczyk E., Davidson A.D., Keller N., Oakley B.R., Wang C.C. A gene cluster containing two fungal polyketide synthases encodes the biosynthetic pathway for a polyketide, asperfuranone, in Aspergillus nidulans. J. Am. Chem. Soc. 2009, 131:2965-2970.
26. Colombo L., Gennari C., Potenza D., Scolastico C., Aragozzini F., Merendi C. Biosynthesis of citrinin and synthesis of its biogenetic precursors. J. Chem. Soc. Perkin Trans. 1981, 1:2594-2597.
27. Colombo L., Gennari C., Scolastico C., Aragozzini F., Merendi C. Biosynthesis of citrinin. J. Chem. Soc. Chem. Commun. 1980, 1132-1134.
28. Cox R.J. Polyketides, proteins and genes in fungi: programmed nano-machines begin to reveal their secrets. Org. Biomol. Chem. 2007, 5:2010-2026.
29. Davison J., al Fahad A., Cai M., Song Z., Yehia S.Y., Lazarus C.M., Bailey A.M., Simpson T.J., Cox R.J. Genetic, molecular, and biochemical basis of fungal tropolone biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:7642-7647.
30. Fujii I., Ebizuka Y., Sankawa U. A novel anthraquinone ring cleavage enzyme from Aspergillus terreus. J. Biochem. 1988, 103:878-883.
31. Fujii I., Ono Y., Tada H., Gomi K., Ebizuka Y., Sankawa U. 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. 1996, 253:1-10.
32. Graminha M.A., Rocha E.M., Prade R.A., Martinez-Rossi N.M. Terbinafine resistance mediated by salicylate 1-monooxygenase in Aspergillus nidulans. Antimicrob. Agents Chemother. 2004, 48:3530-3535.
33. Gressler M., Zaehle C., Scherlach K., Hertweck C., Brock M. Multifactorial induction of an orphan PKS-NRPS gene cluster in Aspergillus terreus. Chem. Biol. 2011, 18:198-209.
34. Guo C.J., Knox B.P., Chiang Y.M., Lo H.C., Sanchez J.F., Lee K.H., Oakley B.R., Bruno K.S., Wang C.C. Molecular genetic characterization of a cluster in A. terreus for biosynthesis of the meroterpenoid terretonin. Org. Lett. 2012, 14:5684-5687.
35. Guo C.J., Yeh H.H., Chiang Y.M., Sanchez J.F., Chang S.L., Bruno K.S., Wang C.C. Biosynthetic pathway for the epipolythiodioxopiperazine acetylaranotin in Aspergillus terreus revealed by genome-based deletion analysis. J. Am. Chem. Soc. 2013, 135:7205-7213.
36. 13C nuclear magnetic resonance. Appl. Environ. Microbiol. 1999, 65:311-314.
37. Han H., Yang Y., Olesen S.H., Becker A., Betzi S., Schönbrunn E. The fungal product terreic acid is a covalent inhibitor of the bacterial cell wall biosynthetic enzyme UDP-N-acetylglucosamine 1-carboxyvinyltransferase (MurA). Biochemistry 2010, 49:4276-4282.
38. Hendrickson L., Davis C.R., Roach C., Nguyen D.K., Aldrich T., McAda P.C., Reeves C.D. Lovastatin biosynthesis in Aspergillus terreus: characterization of blocked mutants, enzyme activities and a multifunctional polyketide synthase gene. Chem. Biol. 1999, 6:429-439.
39. Henry K.M., Townsend C.A. Synthesis and fate of o-carboxybenzophenones in the biosynthesis of aflatoxin. J. Am. Chem. Soc. 2005, 127:3300-3309.
40. Hill R.A., Carter R.H., Staunton J. Biosynthesis of fungal metabolites. Terrein, a metabolite of Aspergillus terreus Thom. J. Chem. Soc. Perkin Trans. 1981, 1:2570-2576.
41. Huang K.X., Fujii I., Ebizuka Y., Gomi K., Sankawa U. Molecular cloning and heterologous expression of the gene encoding dihydrogeodin oxidase, a multicopper blue enzyme from Aspergillus terreus. J. Biol. Chem. 1995, 270:21495-21502.
42. Hutchinson C.R., Kennedy J., Park C., Kendrew S., Auclair K., Vederas J. Aspects of the biosynthesis of non-aromatic fungal polyketides by iterative polyketide synthases. Antonie Van Leeuwenhoek 2000, 78:287-295.
43. Keller N.P., Turner G., Bennett J.W. Fungal secondary metabolism - from biochemistry to genomics. Nat. Rev. Microbiol. 2005, 3:937-947.
44. Kennedy J., Auclair K., Kendrew S.G., Park C., Vederas J.C., Hutchinson C.R. Modulation of polyketide synthase activity by accessory proteins during lovastatin biosynthesis. Science 1999, 284:1368-1372.
45. Li A., van Luijk N., ter Beek M., Caspers M., Punt P., van der Werf M. A clone-based transcriptomics approach for the identification of genes relevant for itaconic acid production in Aspergillus. Fungal Genet. Biol. 2011, 48:602-611.
46. Marchler-Bauer A., Zheng C., Chitsaz F., Derbyshire M.K., Geer L.Y., Geer R.C., Gonzales N.R., Gwadz M., Hurwitz D.I., Lanczycki C.J., Lu F., Lu S., Marchler G.H., Song J.S., Thanki N., Yamashita R.A., Zhang D., Bryant S.H. CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res. 2013, 41(D1):D348-D352.
47. Moriguchi T., Kezuka Y., Nonaka T., Ebizuka Y., Fujii I. Hidden function of catalytic domain in 6-methylsalicylic acid synthase for product release. J. Biol. Chem. 2010, 285:15637-15643.
48. Nielsen M.T., Nielsen J.B., Anyaogu D.C., Holm D.K., Nielsen K.F., Larsen T.O., Mortensen U.H. Heterologous reconstitution of the intact geodin gene cluster in Aspergillus nidulans through a simple and versatile PCR based approach. PLoS ONE 2013, 8(8):e72871.
49. Pažoutová S., Linka M., Štorková Š., Schwab H. Polyketide synthase gene pksM from Aspergillus terreus expressed during growth phase. Folia Microbiol. (Praha) 1997, 42:419-430.
50. Puel O., Galtier P., Oswald I.P. Biosynthesis and toxicological effects of patulin. Toxins (Basel) 2010, 2:613-631.
51. Read G., Westlake D.W., Vining L.C. Quinone epoxides. V. The biosynthesis of terreic acid. Can. J. Biochem. 1969, 47:1071-1079.
52. Sanchez J.F., Somoza A.D., Keller N.P., Wang C.C. Advances in Aspergillus secondary metabolite research in the post-genomic era. Nat. Prod. Rep. 2012, 29:351-371.
53. 17O]-acetate. Tetrahedron 1983, 39:3583-3591.
54. Shimizu T., Kinoshita H., Nihira T. Identification and in vivo functional analysis by gene disruption of ctnA, an activator gene involved in citrinin biosynthesis in Monascus purpureus. Appl. Environ. Microbiol. 2007, 73:5097-5103.
55. Strieker M., Tanović A., Marahiel M.A. Nonribosomal peptide synthetases: structures and dynamics. Curr. Opin. Struct. Biol. 2010, 20:234-240.
56. Sygmund C., Klausberger M., Felice A.K., Ludwig R. Reduction of quinones and phenoxy radicals by extracellular glucose dehydrogenase from Glomerella cingulata suggests a role in plant pathogenicity. Microbiology 2011, 157:3203-3212.
57. The UniProt Consortium Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res. 2013, 41:D43-D47.
58. Varga J., Tóth B., Kocsubé S., Farkas B., Szakács G., Téren J., Kozakiewicz Z. Evolutionary relationships among Aspergillus terreus isolates and their relatives. Antonie Van Leeuwenhoek 2005, 88:141-150.
59. Wang H., Wu Y., Zhao Z. Fragmentation study of simvastatin and lovastatin using electrospray ionization tandem mass spectrometry. J. Mass Spectrom. 2001, 36:58-70.
60. Winter J.M., Behnken S., Hertweck C. Genomics-inspired discovery of natural products. Curr. Opin. Chem. Biol. 2011, 15:22-31.
61. Xu Y., Espinosa-Artiles P., Schubert V., Xu Y.M., Zhang W., Lin M., Gunatilaka A.A., Süssmuth R., Molnár I. Characterization of the biosynthetic genes for 10,11-dehydrocurvularin, a heat shock response-modulating anticancer fungal polyketide from Aspergillus terreus. Appl. Environ. Microbiol. 2013, 79:2038-2047.
62. Zabala A.O., Xu W., Chooi Y.H., Tang Y. Characterization of a silent azaphilone gene cluster from Aspergillus niger ATCC 1015 reveals a hydroxylation-mediated pyran-ring formation. Chem. Biol. 2012, 19:1049-1059.