Identification of a fungal 1,8-cineole synthase from Hypoxylon sp. with specificity determinants in common with the plant synthases

Journal of Biological Chemistry

Volumn 290, Issue 13, 2015, Pages 8511-8526

  Shaw, Jeffrey J ^a   Berbasova, Tetyana ^a   Sasaki, Tomoaki ^a   Jefferson George, Kyra ^b   Spakowicz, Daniel J ^a   Dunican, Brian F ^a   Portero, Carolina E ^c   Narváez Trujillo, Alexandra ^c   Strobel, Scott A ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DEL ECUADOR   (Ecuador)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; MONOTERPENES;

1 ,8-CINEOLE; SYNTHASES;

FUNGI;

1,8 CINEOLE SYNTHASE; 2 METHYL BUTANOL; 2 METHYL PROPANOL; 2 METHYLBUTYL ACETIC ACID; 3 METHYL BUTANOL; ALPHA PHELLANDRENE; FUNGAL ENZYME; HYP3 PROTEIN; INTERNAL TRANSCRIBED SPACER; LIMONENE; NEROLIDOL; PARA CYMENE; PINENE; TERPENE; TERPINENE; TERPINOLENE; UNCLASSIFIED DRUG; 1,8-CINEOLE SYNTHETASE; CINEOLE; CYCLOHEXANOL DERIVATIVE; FUNGAL PROTEIN; LYASE; PLANT PROTEIN; VOLATILE ORGANIC COMPOUND;

AMINO ACID SEQUENCE; ANNULOHYPOXYLON; ARTICLE; CULTURE MEDIUM; CYCLIZATION; DALDINIA; ENDOPHYTIC FUNGUS; ENZYME ACTIVE SITE; ENZYME ASSAY; ENZYME SPECIFICITY; FUNGUS; FUNGUS CULTURE; FUNGUS ISOLATION; GENE EXPRESSION; GENE SEQUENCE; HYPOXYLON; HYPOXYLON MONTICULOSUM; MASS FRAGMENTOGRAPHY; MUTATIONAL ANALYSIS; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; SIGNAL TRANSDUCTION; SOLID PHASE MICROEXTRACTION; STREPTOMYCES CLAVULIGERUS; ASCOMYCETES; CHEMICAL STRUCTURE; CHEMISTRY; ENDOPHYTE; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; MICROBIOLOGY; MISSENSE MUTATION; MOLECULAR GENETICS; PLANT STEM;

HYPOXYLON;

AMINO ACID SEQUENCE; ASCOMYCOTA; CARBON-CARBON LYASES; CYCLOHEXANOLS; ENDOPHYTES; FUNGAL PROTEINS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MONOTERPENES; MUTATION, MISSENSE; PHYLOGENY; PLANT PROTEINS; PLANT STEMS; SUBSTRATE SPECIFICITY; VOLATILE ORGANIC COMPOUNDS;

EID: 84925710324     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.636159     Document Type: Article

References (82)

1. Turner, W. B., and Aldridge, D. C. (1983) Fungal Metabolites, Academic Press, New York
2. Strobel, G., Daisy, B., Castillo, U., and Harper, J. (2004) Natural products from endophytic microorganisms. J. Nat. Prod. 67, 257-268
3. Schulz, B., Boyle, C., Draeger, S., Römmert, A.-K., and Krohn, K. (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol. Res. 106, 996-1004
4. Peralta-Yahya, P. P., and Keasling, J. D. (2010) Advanced biofuel production in microbes. Biotechnol. J. 5, 147-162
5. Fortman, J. L., Chhabra, S., Mukhopadhyay, A., Chou, H., Lee, T. S., Steen, E., and Keasling, J. D. (2008) Biofuel alternatives to ethanol: pumping the microbial well. Trends Biotechnol. 26, 375-381
6. Christianson, D. W. (2008) Unearthing the roots of the terpenome. Curr. Opin. Chem. Biol. 12, 141-150
7. Degenhardt, J., Köllner, T. G., and Gershenzon, J. (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70, 1621-1637
8. Bohlmann, J., Meyer-Gauen, G., and Croteau, R. (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc. Natl. Acad. Sci. U.S.A. 95, 4126-4133
9. Lesburg, C. A., Zhai, G., Cane, D. E., and Christianson, D. W. (1997) Crystal structure of pentalenene synthase: mechanistic insights on terpenoid cyclization reactions in biology. Science 277, 1820-1824
10. Starks, C. M., Back, K., Chappell, J., and Noel, J. P. (1997) Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science 277, 1815-1820
11. Aubourg, S., Lecharny, A., and Bohlmann, J. (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol. Genet. Genomics 267, 730-745
12. Sharkey, T. D., Yeh, S., Wiberley, A. E., Falbel, T. G., Gong, D., and Fernandez, D. E. (2005) Evolution of the isoprene biosynthetic pathway in kudzu. Plant Physiol. 137, 700-712
13. Greenhagen, B. T., O'Maille, P. E., Noel, J. P., and Chappell, J. (2006) Identifying and manipulating structural determinates linking catalytic specificities in terpene synthases. Proc. Natl. Acad. Sci. U.S.A. 103, 9826-9831
14. Lauchli, R., Rabe, K. S., Kalbarczyk, K. Z., Tata, A., Heel, T., Kitto, R. Z., and Arnold, F. H. (2013) High-throughput screening for terpene-synthasecyclization activity and directed evolution of a terpene synthase. Angew. Chem. Int. Ed. 52, 5571-5574
15. Yoshikuni, Y., Ferrin, T. E., and Keasling, J. D. (2006) Designed divergent evolution of enzyme function. Nature 440, 1078-1082
16. Kampranis, S. C., Ioannidis, D., Purvis, A., Mahrez, W., Ninga, E., Katerelos, N. A., Anssour, S., Dunwell, J. M., Degenhardt, J., Makris, A. M., Goodenough, P. W., and Johnson, C. B. (2007) Rational conversion of substrate and product specificity in a Salvia monoterpene synthase: structural insights into the evolution of terpene synthase function. Plant Cell 19, 1994-2005
17. 2+ B motif,. Arch. Biochem. Biophys. 469, 184-194
18. Trombetta, D., Castelli, F., Sarpietro, M. G., Venuti, V., Cristani, M., Daniele, C., Saija, A., Mazzanti, G., and Bisignano, G. (2005) Mechanisms of antibacterial action of three monoterpenes. Antimicrob. Agents Chemother. 49, 2474-2478
19. Inoue, Y., Shiraishi, A., Hada, T., Hirose, K., Hamashima, H., and Shimada, J. (2004) The antibacterial effects of terpene alcohols on Staphylococcus aureus and their mode of action. FEMS Microbiol. Lett. 237, 325-331
20. Haynes, R. K. (2001) Artemisinin and derivatives: the future for malaria treatment? Curr. Opin. Infect. Dis. 14, 719-726
21. Jennewein, S., and Croteau, R. (2001) Taxol: biosynthesis, molecular genetics, and biotechnological applications. Appl. Microbiol. Biotechnol. 57, 13-19
22. Peralta-Yahya, P. P., Ouellet, M., Chan, R., Mukhopadhyay, A., Keasling, J. D., and Lee, T. S. (2011) Identification and microbial production of a terpene-based advanced biofuel. Nat. Commun. 2, 483
23. Alonso-Gutierrez, J., Chan, R., Batth, T. S., Adams, P. D., Keasling, J. D., Petzold, C. J., and Lee, T. S. (2013) Metabolic engineering of Escherichia coli for limonene and perillyl alcohol production. Metab. Eng. 19, 33-41
24. Harvey, B. G., Wright, M. E., and Quintana, R. L. (2010) High-density renewable fuels based on the selective dimerization of pinenes. Energy Fuels 24, 267-273
25. Yang, J., Nie, Q., Ren, M., Feng, H., Jiang, X., Zheng, Y., Liu, M., Zhang, H., and Xian, M. (2013) Metabolic engineering of Escherichia coli for the biosynthesis of α-pinene. Biotechnol. Biofuels 6, 60
26. Dietrich, J. A., Yoshikuni, Y., Fisher, K. J., Woolard, F. X., Ockey, D., McPhee, D. J., Renninger, N. S., Chang, M. C. Y., Baker, D., and Keasling, J. D. (2009) A novel semi-biosynthetic route for artemisinin production using engineered substrate-promiscuous P450BM3. ACS Chem. Biol. 4, 261-267
27. Martin, V. J. J., Pitera, D. J., Withers, S. T., Newman, J. D., and Keasling, J. D. (2003) Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat. Biotechnol. 21, 796-802
28. Redding-Johanson, A. M., Batth, T. S., Chan, R., Krupa, R., Szmidt, H. L., Adams, P. D., Keasling, J. D., Lee, T. S., Mukhopadhyay, A., and Petzold, C. J. (2011) Targeted proteomics for metabolic pathway optimization: application to terpene production. Metab. Eng. 13, 194-203
29. Blackwell, M. (2011) The Fungi: 1, 2, 3. 5.1 million species? Am. J. Bot. 98, 426-438
30. Cane, D. E., Shim, J. H., Xue, Q., Fitzsimons, B. C., and Hohn, T. M. (1995) Trichodiene synthase: identification of active site residues by site-directed mutagenesis. Biochemistry 34, 2480-2488
31. Hohn, T. M., and Plattner, R. D. (1989) Purification and characterization of the sesquiterpene cyclase aristolochene synthase from Penicillium roqueforti. Arch. Biochem. Biophys. 272, 137-143
32. Hohn, T. M., and Beremand, P. D. (1989) Isolation and nucleotide sequence of a sesquiterpene cyclase gene from the trichothecene-producing fungus Fusarium sporotrichioides. Gene 79, 131-138
33. Pinedo, C., Wang, C.-M., Pradier, J.-M., Dalmais, B., Choquer, M., Le Pecheur, P., Morgant, G., Collado, I. G., Cane, D. E., and Viaud, M. (2008) Sesquiterpene synthase from the botrydial biosynthetic gene cluster of the phytopathogen Botrytis cinerea. ACS Chem. Biol. 3, 791-801
34. Agger, S., Lopez-Gallego, F., and Schmidt-Dannert, C. (2009) Diversity of sesquiterpene synthases in the basidiomycete Coprinus cinereus. Mol. Microbiol. 72, 1181-1195
35. Wawrzyn, G. T., Quin, M. B., Choudhary, S., López-Gallego, F., and Schmidt-Dannert, C. (2012) Draft genome of Omphalotus olearius provides a predictive framework for sesquiterpenoid natural product biosynthesis in Basidiomycota. Chem. Biol. 19, 772-783
36. Engels, B., Heinig, U., Grothe, T., Stadler, M., and Jennewein, S. (2011) Cloning and Characterization of an Armillaria gallica cDNA encoding protoilludene synthase, which catalyzes the first committed step in the synthesis of antimicrobial melleolides. J. Biol. Chem. 286, 6871-6878
37. Griffin, M. A., Spakowicz, D. J., Gianoulis, T. A., and Strobel, S. A. (2010) Volatile organic compound production by organisms in the genus Ascocoryne and a re-evaluation of myco-diesel production by NRRL 50072. Microbiology 156, 3814-3829
38. Riyaz-Ul-Hassan, S., Strobel, G., Geary, B., and Sears, J. (2013) An endophytic Nodulisporium sp. from Central America producing volatile organic compounds with both biological and fuel potential. J. Microbiol. Biotechnol. 23, 29-35
39. Tess Mends, M., and Yu, E. (2012) An Endophytic Nodulisporium sp. producing volatile organic compounds having bioactivity and fuel potential. J. Pet. Environ. Biotechnol. 10.4172/2157-7463.1000117
40. Tomsheck, A. R., Strobel, G. A., Booth, E., Geary, B., Spakowicz, D., Knighton, B., Floerchinger, C., Sears, J., Liarzi, O., and Ezra, D. (2010) Hypoxylon sp., an endophyte of Persea indica, producing 1,8-cineole and other bioactive volatiles with fuel potential. Microb. Ecol. 60, 903-914
41. Silvestre, A. J. D., Válega, M., and Cavaleiro, J. A. S. (2000) Chemical transformation of 1,8-cineole: synthesis of seudenone, an insect pheromone. Ind. Crops Prod. 10.1016/S0926-6690(99)00067-9
42. Silvestre, A. J. D., Cavaleiro, J. A. S., Feio, S. S., Roseiro, J. C., Delmond, B., and Filliatre, C. (1999) Synthesis of some new benzylic ethers from 1,8- cineole with antimicrobial activity. Monatshefte Für Chem. Chem. Mon. 130, 589-595
43. Leita, B. A., Gray, P., O'Shea, M., Burke, N., Chiang, K., and Trimm, D. (2011) The conversion of 1,8-cineole sourced from renewable eucalyptus oil to p-cymene over a palladium doped γ-Al2O3 catalyst. Catal. Today 10.1016/j.cattod.2011.05.037
44. Barton, A. F. M., and Tjandra, J. (1989) Eucalyptus oil as a cosolvent in water-ethanol-gasoline mixtures. Fuel 10.1016/0016-2361(89)90004-5
45. Strobel, G. A., Knighton, B., Kluck, K., Ren, Y., Livinghouse, T., Griffin, M., Spakowicz, D., and Sears, J. (2008) The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum (NRRL 50072). Microbiology 154, 3319-3328
46. Ezra, D., Hess, W. M., and Strobel, G. A. (2004) New endophytic isolates of Muscodor albus, a volatile-antibiotic-producing fungus. Microbiology 150, 4023-4031
47. Van Zeijl, C. M. J., van de Kamp, E. H. M., Punt, P. J., Selten, G. C. M., Hauer, B., van Gorcom, R. F. M., and van den Hondel, C. A. M. J. J. (1997) An improved colony-PCR method for filamentous fungi for amplification of PCR-fragments of several kilobases. J. Biotechnol. 59, 221-224
48. White, T. J., Bruns, T., Lee, S., and Taylor, J. (1990) in PCR Protocols: A Guide to Methods and Application, pp. 315-322, Academic Press, New York
49. Suwannasai, N., Martín, M. P., Phosri, C., Sihanonth, P., Whalley, A. J. S., and Spouge, J. L. (2013) Fungi in Thailand: A Case Study of the Efficacy of an ITS Barcode for Automatically Identifying Species within the Annulohypoxylon and Hypoxylon Genera. PLoS One 8, e54529
50. Hsieh, H.-M., Ju, Y.-M., and Rogers, J. D. (2005) Molecular phylogeny of Hypoxylon and closely related genera. Mycologia 97, 844-865
51. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690
52. Ronquist, F., and Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574
53. Gianoulis, T. A., Griffin, M. A., Spakowicz, D. J., Dunican, B. F., Alpha, C. J., Sboner, A., Sismour, A. M., Kodira, C., Egholm, M., Church, G. M., Gerstein, M. B., and Strobel, S. A. (2012) Genomic analysis of the hydrocarbon- producing, cellulolytic, endophytic fungus Ascocoryne sarcoides. PLoS Genet. 8, e1002558
54. Gnerre, S., Maccallum, I., Przybylski, D., Ribeiro, F. J., Burton, J. N., Walker, B. J., Sharpe, T., Hall, G., Shea, T. P., Sykes, S., Berlin, A. M., Aird, D., Costello, M., Daza, R., Williams, L., Nicol, R., Gnirke, A., Nusbaum, C., Lander, E. S., and Jaffe, D. B. (2011) High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl. Acad. Sci. U.S.A. 108, 1513-1518
55. Newman, J. D., Marshall, J., Chang, M., Nowroozi, F., Paradise, E., Pitera, D., Newman, K. L., and Keasling, J. D. (2006) High-level production of amorpha-4,11-diene in a two-phase partitioning bioreactor of metabolically engineered Escherichia coli. Biotechnol. Bioeng. 95, 684-691
56. Horton, P., Park, K.-J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C. J., and Nakai, K. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35, W585-W587
57. Horton, P., and Nakai, K. (1997) Better prediction of protein cellular localization sites with the k nearest neighbors classifier. Proc. Int. Conf. Intell. Syst. Mol. Biol. 5, 147-152
58. Shishova, E. Y., Di Costanzo, L., Cane, D. E., and Christianson, D. W. (2007) X-ray crystal structure of aristolochene synthase from Aspergillus terreus and evolution of templates for the cyclization of farnesyl diphosphate. Biochemistry 46, 1941-1951
59. Fiser, A., and Sali, A. (2003) Modeller: generation and refinement of homology- based protein structure models. Methods Enzymol. 374, 461-491
60. Nakano, C., Kim, H.-K., and Ohnishi, Y. (2011) Identification of the first bacterial monoterpene cyclase, a 1,8-cineole synthase, that catalyzes the direct conversion of geranyl diphosphate. Chembiochem 12, 1988-1991
61. Felicetti, B., and Cane, D. E. (2004) Aristolochene synthase: mechanistic analysis of active site residues by site-directed mutagenesis. J. Am. Chem. Soc. 126, 7212-7221
62. Chen, M., Al-lami, N., Janvier, M., D'Antonio, E. L., Faraldos, J. A., Cane, D. E., Allemann, R. K., and Christianson, D. W. (2013) Mechanistic insights from the binding of substrate and carbocation intermediate analogues to aristolochene synthase. Biochemistry 52, 5441-5453
63. Carter, O. A., Peters, R. J., and Croteau, R. (2003) Monoterpene biosynthesis pathway construction in Escherichia coli. Phytochemistry 64, 425-433
64. Davis, E. M., and Croteau, R. (2000) Cyclization Enzymes in the Biosynthesis of Monoterpenes, Sesquiterpenes, and Diterpenes. Top. Curr. Chem. 10.1007/3-540-48146-X-2
65. Degenhardt, J., and Gershenzon, J. (2000) Demonstration and characterization of (E)-nerolidol synthase from maize: a herbivore-inducible terpene synthase participating in (3E)-4,8-dimethyl-1,3,7-nonatriene biosynthesis. Planta 210, 815-822
66. Benedict, C. R., Alchanati, I., Harvey, P. J., Liu, J., Stipanovic, R. D., and Bell, A. A. (1995) The enzymatic formation of δ-cadinene from farnesyl diphosphate in extracts of cotton. Phytochemistry 10.1016/0031-9422(95)00066-G
67. Chen, X.-Y., Chen, Y., Heinstein, P., and Davisson, V. J. (1995) Cloning, expression, and characterization of (+)- δ-cadinene synthase: a catalyst for cotton phytoalexin biosynthesis. Arch. Biochem. Biophys. 324, 255-266
68. Kumeta, Y., and Ito, M. (2010) Characterization of δ-guaiene synthases from cultured cells of Aquilaria, responsible for the formation of the sesquiterpenes in agarwood. Plant Physiol. 154, 1998-2007
69. Fähnrich, A., Krause, K., and Piechulla, B. (2011) Product variability of the "cineole cassette" monoterpene synthases of related Nicotiana species. Mol. Plant. 4, 965-984
70. Fähnrich, A., Brosemann, A., Teske, L., Neumann, M., and Piechulla, B. (2012) Synthesis of "cineole cassette" monoterpenes in Nicotiana section alatae: gene isolation, expression, functional characterization and phylogenetic analysis. Plant Mol. Biol. 79, 537-553
71. Croteau, R., Alonso, W. R., Koepp, A. E., and Johnson, M. A. (1994) Biosynthesis of monoterpenes: partial purification, characterization, and mechanism of action of 1,8-cineole synthase. Arch. Biochem. Biophys. 309, 184-192
72. Xu, M., Wilderman, P. R., and Peters, R. J. (2007) Following evolution's lead to a single residue switch for diterpene synthase product outcome. Proc. Natl. Acad. Sci. U.S.A. 104, 7397-7401
73. Wilderman, P. R., and Peters, R. J. (2007) A single residue switch converts abietadiene synthase into a pimaradiene specific cyclase. J. Am. Chem. Soc. 129, 15736-15737
74. Keeling, C. I., Weisshaar, S., Lin, R. P. C., and Bohlmann, J. (2008) Functional plasticity of paralogous diterpene synthases involved in conifer defense. Proc. Natl. Acad. Sci. U.S.A. 105, 1085-1090
75. Katoh, S., Hyatt, D., and Croteau, R. (2004) Altering product outcome in Abies grandis (-)-limonene synthase and (-)-limonene/(-)-α-pinene synthase by domain swapping and directed mutagenesis. Arch. Biochem. Biophys. 425, 65-76
76. Köllner, T. G., Held, M., Lenk, C., Hiltpold, I., Turlings, T. C. J., Gershenzon, J., and Degenhardt, J. (2008) A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most american maize varieties. Plant Cell 20, 482-494
77. Pichersky, E., and Gang, D. R. (2000) Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective. Trends Plant Sci. 5, 439-445
78. Cane, D. E., and Ikeda, H. (2012) Exploration and mining of the bacterial terpenome. Acc. Chem. Res. 45, 463-472
79. Wawrzyn, G. T., Bloch, S. E., and Schmidt-Dannert, C. (2012) Discovery and characterization of terpenoid biosynthetic pathways of fungi. Methods Enzymol. 515, 83-105
80. Wang, J. L., Li, Y., and Lei, C. L. (2009) Evaluation of monoterpenes for the control of Tribolium castaneum (Herbst) and Sitophilus zeamaise Motschulsky. Nat. Prod. Res. 23, 1080-1088
81. Klocke, J. A., Darlington, M. V., and Balandrin, M. F. (1987) 1,8-Cineole (Eucalyptol), a mosquito feeding and ovipositional repellent from volatile oil of Hemizonia fitchii (Asteraceae). J. Chem. Ecol. 13, 2131-2141
82. Shaw, J. J., Spakowicz, D. J., Dalal, R. S., Davis, J. H., Lehr, N. A., Dunican, B. F., Orellana, E. A., Narváez-Trujillo, A., and Strobel, S. A. (2015) Biosynthesis and genomic analysis of medium-chain hydrocarbon production by the endophytic fungal isolate Nigrograna mackinnonii E5202H. Appl. Microbiol. Biotechnol. 10.1007/s00253-014-6206-5