Identification and functional characterization of the CYP51 gene from the yeast Xanthophyllomyces dendrorhous that is involved in ergosterol biosynthesis

BMC Microbiology

Volumn 15, Issue 1, 2015, Pages

  Leiva, Kritsye ^a   Werner, Nicole ^a   Sepúlveda, Dionisia ^a   Barahona, Salvador ^a   Baeza, Marcelo ^a   Cifuentes, Víctor ^a   Alcaíno, Jennifer ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

Astaxanthin; Cytochrome P450 enzyme systems (P450); Sterol C14 demethylase; Sterols

Indexed keywords

AMINO ACID; C 14 DEMETHYLASE; CYTOCHROME P450; CYTOCHROME P450 REDUCTASE; ERGOSTEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; STEROL 14ALPHA DEMETHYLASE; UNCLASSIFIED DRUG; UNCLASSIFIED ENZYME; CAROTENOID; FUNGAL DNA;

ARTICLE; CONTROLLED STUDY; CYP51 GENE; ESTROGEN SYNTHESIS; EXON; FUNGUS; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; GENE SEQUENCE; GENETIC TRANSCRIPTION; LIPOGENESIS; NONHUMAN; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE; XANTHOPHYLLOMYCES DENDRORHOUS; BASIDIOMYCETES; BIOSYNTHESIS; CHEMISTRY; DNA SEQUENCE; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; SEQUENCE HOMOLOGY;

FUNGI; XANTHOPHYLLOMYCES DENDRORHOUS;

BASIDIOMYCOTA; CAROTENOIDS; DNA, FUNGAL; ERGOSTEROL; EXONS; GENETIC COMPLEMENTATION TEST; MOLECULAR SEQUENCE DATA; MUTATION; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; STEROL 14-DEMETHYLASE;

EID: 84928573043     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/s12866-015-0428-2     Document Type: Article

References (64)

1. The Global Market for Carotenoids. Report Code: FOD025D. [ http://www.bccresearch.com/pressroom/fod/global-carotenoids-market-reach-11th4-billion-2018 ]
2. Schmidt I, Schewe H, Gassel S, Jin C, Buckingham J, Hümbelin M, et al. Biotechnological production of astaxanthin with Phaffia rhodozyma/Xanthophyllomyces dendrorhous. Appl Microbiol Biotechnol. 2011;89:555-71.
3. Schroeder WA, Johnson EA. Antioxidant role of carotenoids in Phaffia rhodozyma. J Gen Microbiol. 1993;139:907-12.
4. Schroeder WA, Johnson EA. Carotenoids protect Phaffia rhodozyma against singlet oxygen damage. J Ind Microbiol. 1995;14:502-7.
5. Schroeder WA, Johnson EA. Singlet oxygen and peroxyl radicals regulate carotenoid biosynthesis in Phaffia rhodozyma. J Biol Chem. 1995;270:18374-9.
6. Wang X, Willen R, Wadstrom T. Astaxanthin-rich algal meal and vitamin C inhibit Helicobacterpylori infection in BALB/cA mice. Antimicrob Agents Chemother. 2000;44:2452-7.
7. Higuera-Ciapara I, Felix-Valenzuela L, Goycoolea FM. Astaxanthin: a review of its chemistry and applications. CRC Crit Rev Food Sci Nutr. 2006;46:185-96.
8. Park JS, Chyun JH, Kim YK, Line LL, Chew BP. Astaxanthin decreased oxidative stress and inflammation and enhanced immune response in humans. Nutr Metab. 2010;7:18.
9. Yasui Y, Hosokawa M, Mikami N, Miyashita K, Tanaka T. Dietary astaxanthin inhibits colitis and colitis-associated colon carcinogenesis in mice via modulation of the inflammatory cytokines. Chem Biol Interact. 2011;193:79-87.
10. Alvarez V, Rodriguez-Saiz M, de la Fuente JL, Gudina EJ, Godio RP, Martin JF, et al. The crtS gene of Xanthophyllomyces dendrorhous encodes a novel cytochrome-P450 hydroxylase involved in the conversion of beta-carotene into astaxanthin and other xanthophylls. Fungal Genet Biol. 2006;43:261-72.
11. Ojima K, Breitenbach J, Visser H, Setoguchi Y, Tabata K, Hoshino T, et al. Cloning of the astaxanthin synthase gene from Xanthophyllomyces dendrorhous (Phaffia rhodozyma) and its assignment as a beta-carotene 3-hydroxylase/4-ketolase. Mol Genet Genomics. 2006;275:148-58.
12. Alcaino J, Barahona S, Carmona M, Lozano C, Marcoleta A, Niklitschek M, et al. Cloning of the cytochrome p450 reductase (crtR) gene and its involvement in the astaxanthin biosynthesis of Xanthophyllomyces dendrorhous. BMC Microbiol. 2008;8:169.
13. Csernetics A, Toth E, Farkas A, Nagy G, Bencsik O, Vagvolgyi C, et al. Expression of Xanthophyllomyces dendrorhous cytochrome-P450 hydroxylase and reductase in Muco rcircinelloides. World J Microbiol Biotechnol. 2015;31:321-36.
14. Zhang H, Im S-C, Waskell L. Cytochrome b5 increases the rate of product formation by cytochrome P450 2B4 and competes with cytochrome P450 reductase for a binding site on cytochrome P450 2B4. J Biol Chem. 2007;282:29766-76.
15. Degtyarenko KN, Archakov AI. Molecular evolution of P450 superfamily and P450-containing monooxygenase systems. FEBS Lett. 1993;332:1-8.
16. Bernhardt R. Cytochromes P450 as versatile biocatalysts. J Biotechnol. 2006;124:128-45.
17. Estabrook RW. A passion for P450s (remembrances of the early history of research on cytochrome P450). Drug Metab Dispos. 2003;31:1461-73.
18. Porter TD, Coon MJ. Cytochrome P-450. Multiplicity of isoforms, substrates, and catalytic and regulatory mechanisms. J Biol Chem. 1991;266:13469-72.
19. Kimmich N, Das A, Sevrioukova I, Meharenna Y, Sligar SG, Poulos TL. Electron transfer between cytochrome P450cin and its FMN-containing redox partner, cindoxin. J Biol Chem. 2007;282:27006-11.
20. Loto I, Gutiérrez MS, Barahona S, Sepúlveda D, Martínez-Moya P, Baeza M, et al. Enhancement of carotenoid production by disrupting the C22-sterol desaturase gene (CYP61) in Xanthophyllomyces dendrorhous. BMC Microbiol. 2012;12:235.
21. Kelly SL, Kelly DE. Microbial cytochromes P450: biodiversity and biotechnology. Where do cytochromes P450 come from, what do they do and what can they do for us? Philos Trans R Soc Lond B Biol Sci. 2013;368:20120476.
22. Aoyama Y, Yoshida Y, Sato R. Yeast cytochrome P-450 catalyzing lanosterol 14 alpha-demethylation. II. Lanosterol metabolism by purified P-450(14)DM and by intact microsomes. J Biol Chem. 1984;259:1661-6.
23. Kalb VF, Woods CW, Turi TG, Dey CR, Sutter TR, Loper JC. Primary structure of the P450 lanosterol demethylase gene from Saccharomyces cerevisiae. DNA. 1987;6:529-37.
24. Werck-Reichhart D, Feyereisen R. Cytochromes P450: a success story. Genome Biol. 2000;1:3003.1-9.
25. Fischer M, Knoll M, Sirim D, Wagner F, Funke S, Pleiss J. The Cytochrome P450 Engineering Database: a navigation and prediction tool for the cytochrome P450 protein family. Bioinformatics. 2007;23:2015-7.
26. Sirim D, Wagner F, Lisitsa A, Pleiss J. The cytochrome P450 engineering database: Integration of biochemical properties. BMC Biochem. 2009;10:27.
27. Shimizu T, Tateishi T, Hatano M, Fujii-Kuriyama Y. Probing the role of lysines and arginines in the catalytic function of cytochrome P450d by site-directed mutagenesis. Interaction with NADPH-cytochrome P450 reductase. J Biol Chem. 1991;266:3372-5.
28. Hatae T, Hara S, Yokoyama C, Yabuki T, Inoue H, Ullrich V, et al. Site-directed mutagenesis of human prostacyclin synthase: Alteration of Cys441 of the Cys-pocket, and Glu347 and Arg350 of the EXXR motif. FEBS Lett. 1996;389:268-72.
29. Syed K, Mashele SS. Comparative analysis of P450 signature motifs EXXR and CXG in the large and diverse kingdom of fungi: identification of evolutionarily conserved amino acid patterns characteristic of P450 family. PLoS One. 2014;9:e95616.
30. van den Brink HM, van Gorcom RF, van den Hondel CA, Punt PJ. Cytochrome P450 enzyme systems in fungi. Fungal Genet Biol. 1998;23:1-17.
31. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, et al. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J Comput Chem. 2009;30:2785-91.
32. Sharma V, Bhatia R. Triazoles in Antifungal Therapy: A Review. Int J Res Pharm Biomed. 2011;2:417-27.
33. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science. 1999;285:901-6.
34. Dawes IW, Hardie ID. Selective killing of vegetative cells in sporulated yeast cultures by exposure to diethyl ether. Mol Gen Genet. 1974;131:281-9.
35. Alcaino J, Romero I, Niklitschek M, Sepulveda D, Rojas MC, Baeza M, et al. Functional characterization of the Xanthophyllomyces dendrorhous farnesyl pyrophosphate synthase and geranylgeranyl pyrophosphate synthase encoding genes that are involved in the synthesis of isoprenoid precursors. PLoS One. 2014;9:e96626.
36. Lepesheva GI, Waterman MR. Sterol 14alpha-demethylase cytochrome P450 (CYP51), a P450 in all biological kingdoms. Biochim Biophys Acta. 2007;1770:467-77.
37. Zill G, Engelhardt G, Wallnöfer PR. Determination of ergosterol as a measure of fungal growth using Si 60 HPLC. Z Lebensm Unters For. 1988;187:246-9.
38. Lodato P, Alcaino J, Barahona S, Retamales P, Jimenez A, Cifuentes V. Study of the expression of carotenoid biosynthesis genes in wild-type and deregulated strains of Xanthophyllomyces dendrorhous (Ex.: Phaffia rhodozyma). Biol Res. 2004;37:83-93.
39. Wozniak A, Lozano C, Barahona S, Niklitschek M, Marcoleta A, Alcaíno J, et al. Differential carotenoid production and gene expression in Xanthophyllomyces dendrorhous grown in a nonfermentable carbon source. FEMS Yeast Res. 2011;11:252-62.
40. Marcoleta A, Niklitschek M, Wozniak A, Lozano C, Alcaino J, Baeza M, et al. Glucose and ethanol-dependent transcriptional regulation of the astaxanthin biosynthesis pathway in Xanthophyllomyces dendrorhous. BMC Microbiol. 2011;11:190.
41. Verdoes JC, Sandmann G, Visser H, Diaz M, van Mossel M, van Ooyen AJ. Metabolic engineering of the carotenoid biosynthetic pathway in the yeast Xanthophyllomyces dendrorhous (Phaffia rhodozyma). Appl Environ Microbiol. 2003;69:3728-38.
42. Miao L, Chi S, Tang Y, Su Z, Yin T, Guan G, et al. Astaxanthin biosynthesis is enhanced by high carotenogenic gene expression and decrease of fatty acids and ergosterol in a Phaffia rhodozyma mutant strain. FEMS Yeast Res. 2011;11:192-201.
43. Calo P, de Miguel T, Velázquez JB, Villa TG. Mevalonic acid increases trans-astaxanthin and carotenoid biosynthesis in Phaffia rhodozyma. Biotechnol Lett. 1995;17:575-8.
44. Shimada H, Kondo K, Fraser PD, Miura Y, Saito T, Misawa N. Increased carotenoid production by the food yeast Candida utilis through metabolic engineering of the isoprenoid pathway. Appl Environ Microbiol. 1998;64:2676-80.
45. Parks LW, Casey WM. Physiological implications of sterol biosynthesis in yeast. Annu Rev Microbiol. 1995;49:95-116.
46. Tang Q, Li Y, Yuan QP. Effects of an ergosterol synthesis inhibitor on gene transcription of terpenoid biosynthesis in Blakeslea trispora. Curr Microbiol. 2008;57:527-31.
47. Sambrook J, Russell DW. Molecular Cloning a laboratory manual. New York, United States: Cold Spring Harbor; 2001.
48. Sanchez-Torres P, Gonzalez-Candelas L, Ramon D. Heterologous Expression of a Candida molischiana Anthocyanin-beta-glucosidase in a Wine Yeast Strain. J Agric Food Chem. 1998;46:354-60.
49. Cifuentes V, Hermosilla G, Martinez C, Leon R, Pincheira G, Jimenez A. Genetics and electrophoretic karyotyping of wild-type and astaxanthin mutant strains of Phaffia rhodozyma. Antonie Van Leeuwenhoek. 1997;72:111-7.
50. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156-9.
51. Boyle JS, Lew AM. An inexpensive alternative to glassmilk for DNA purification. Trends Genet. 1995;11:8.
52. Hofmann K, Stoffel W. TMbase-A database of membrane spanning protein segments. Biol Chem H-S. 1993;374:166.
53. Zdobnov EM, Apweiler R. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics. 2001;17:847-8.
54. Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 2014;42:W252-8.
55. Humphrey W, Dalke A, Schulten K. VMD: Visual Molecular Dynamics. J Mol Graph. 1996;14:33-8.
56. Niklitschek M, Alcaíno J, Barahona S, Sepúlveda D, Lozano C, Carmona M, et al. Genomic organization of the structural genes controlling the astaxanthin biosynthesis pathway of Xanthophyllomyces dendrorhous. Biol Res. 2008;41:93-108.
57. Adrio JL, Veiga M. Transformation of the astaxanthin-producing yeast Phaffia rhodozyma. Biotechnol Tech. 1995;9:509-12.
58. Kim IG, Nam SK, Sohn JH, Rhee SK, An GH, Lee SH, et al. Cloning of the ribosomal protein L41 gene of Phaffia rhodozyma and its use as a drug resistance marker for transformation. Appl Environ Microbiol. 1998;64:1947-9.
59. Sherman F. Getting started with yeast. Methods Enzymol. 2002;350:3-41.
60. Shang F, Wen S, Wang X, Tan T. Effect of nitrogen limitation on the ergosterol production by fed-batch culture of Saccharomyces cerevisiae. J Biotechnol. 2006;122:285-92.
61. An GH, Schuman DB, Johnson EA. Isolation of Phaffia rhodozyma mutants with increased astaxanthin content. Appl Environ Microbiol. 1989;55:116-24.
62. Lodato P, Alcaíno J, Barahona S, Niklitschek M, Carmona M, Wozniak A, et al. Expression of the carotenoid biosynthesis genes in Xanthophyllomyces dendrorhous. Biol Res. 2007;40:73.
63. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-8.
64. Mortimer RK, Johnston JR. Genealogy of principal strains of the yeast genetic stock center. Genetics. 1986;113:35-43.