Identification of sesquiterpene synthases from Nostoc punctiforme PCC 73102 and Nostoc sp. strain PCC 7120

Journal of Bacteriology

Volumn 190, Issue 18, 2008, Pages 6084-6096

  Agger, Sean A ^a   Lopez Gallego, Fernando ^a   Hoye, Thomas R ^b   Schmidt Dannert, Claudia ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b University of Minnesota   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; EUDESMADIENE 8A EPI ALPHA SELINENE; FERREDOXIN REDUCTASE; GEOSMIN; GERMACRADIENOL; GERMACRENE A; OXIDOREDUCTASE; SYNTHETASE; TERPENE; TERPENE SYNTHASE NP1; TERPENE SYNTHASE NP2; TERPENE SYNTHASE NS1; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; ENZYME ANALYSIS; ESCHERICHIA COLI; GENE EXPRESSION; GENE LOCATION; ISOPTERA; NONHUMAN; NOSTOC; NOSTOC PUNCTIFORME; NUCLEOTIDE SEQUENCE; OXYGENATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY; STREPTOMYCES;

ALKYL AND ARYL TRANSFERASES; BACTERIAL PROTEINS; CLONING, MOLECULAR; CYTOCHROME P-450 ENZYME SYSTEM; ESCHERICHIA COLI; GENE EXPRESSION; KINETICS; NOSTOC; OPEN READING FRAMES; RECOMBINANT PROTEINS; SESQUITERPENES;

CYANOBACTERIA; ESCHERICHIA COLI; ISOPTERA; NOSTOC; NOSTOC PUNCTIFORME; NOSTOC PUNCTIFORME PCC 73102; NOSTOC SP.; NOSTOC SP. PCC 7120; STREPTOMYCES;

EID: 51549101817     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00759-08     Document Type: Article

References (55)

1. Adio, A. M., C. Paul, H. Tesso, P. Kolth, and W. A. Koenig. 2004. Absolute configuration of helminthogermacrene. Tetrahedron Asymmetry 15:1631-1635.
2. Ando, M., K. Kikuchi, K. Isogai, T. Ishiwatari, N. Hirata, and H. Yamazaki. 1994. Synthetic studies of sesquiterpenes with a cis-fused decalin system. J. Nat. Prod. 57:1889-1899.
3. Ashby, M. K., and J. Houmard. 2006. Cyanobacterial two-component proteins: structure, diversity, distribution, and evolution. Microbiol. Mol. Biol. Rev. 70:472-509.
4. Bertea, C. M., A. Voster, F. W. Verstappen, M. Maffei, J. Beekwilder, and H. J. Bouwmeester. 2006. Isoprenoid biosynthesis in Artemisia annua: cloning and heterologous expression of a germacrene A synthase from a glandular trichome cDNA library. Arch. Biochem. Biophys. 448:3-12.
5. Bouwmeester, H. J., J. Kodde, F. W. A. Verstappen, I. G. Altug, J. W. de Kraker, and T. E. Wallaart. 2002. Isolation and characterization of two germacrene A synthase cDNA clones from chicory. Plant Physiol. 129:134-144.
6. Calvert, M. J., P. R. Ashton, and R. K. Allemann. 2002. Germacrene A is a product of the aristolochene synthase-mediated conversion of farnesylpyrophosphate to aristolochene. J. Am. Chem. Soc. 124:11636- 11641.
7. Cane, D. E., X. He, S. Kobayashi, S. Omura, and H. Ikeda. 2006. Geosmin biosynthesis in Streptomyces avermitilis. Molecular cloning, expression, and mechanistic study of the germacradienol/geosmin synthase. J. Antibiot. (Tokyo) 59:471-479.
8. Cane, D. E., J. K. Sohng, C. R. Lamberson, S. M. Rudnicki, Z. Wu, M. D. Lloyd, J. S. Oliver, and B. R. Hubbard. 1994. Pentalenene synthase. Purification, molecular cloning, sequencing, and high-level expression in Escherichia coli of a terpenoid cyclase from Streptomyces UC5319. Biochemistry 33:5846-5857.
9. Cane, D. E., and R. M. Watt. 2003. Expression and mechanistic analysis of a germacradienol synthase from Streptomyces coelicolor implicated in geosmin biosynthesis. Proc. Natl. Acad. Sci. USA 100:1547-1551.
10. Carter, O. A., R. J. Peters, and R. Croteau. 2003. Monoterpene biosynthesis pathway construction in Escherichia coli. Phytochemistry 64:425-433.
11. Caruthers, J. M., I. Kang, M. J. Rynkiewicz, D. E. Cane, and D. W. Christianson. 2000. Crystal structure determination of aristolochene synthase from the blue cheese mold, Penicillium roqueforti. J. Biol. Chem. 275:25533-25539.
12. Croteau, R. B., J. J. Shaskus, B. Renstrom, N. M. Felton, D. E. Cane, A. Saito, and C. Chang. 1985. Mechanism of the pyrophosphate migration in the enzymatic cyclization of geranyl and linalyl pyrophosphates to (+)- and (-)-bornyl pyrophosphates. Biochemistry 24:7077-7085.
13. Dairi, T., Y. Hamano, T. Kuzuyama, N. Itoh, K. Furihata, and H. Seto. 2001. Eubacterial diterpene cyclase genes essential for production of the isoprenoid antibiotic terpentecin. J. Bacteriol. 183:6085-6094.
14. Davis, E. M., and R. Croteau. 2000. Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes, and diterpenes. Biosynthesis Aromatic Polyketides Isoprenoids Alkaloids 209:53-95.
15. de Kraker, J. W., H. J. Bouwmeester, M. C. Franssen, and A. de Groot. 1999. (+)-Germacrene A synthesis in chicory (Cichorium intybus L.); the first step in sesquiterpene lactone biosynthesis. Acta Bot. Gallica 146:111-115.
16. +-dependent sesquiterpenoid dehydrogenase(s) involved in sesquiterpene lactone biosynthesis. Plant Physiol. 125:1930-1940.
17. Faraldos, J. A., Y. Zhao, P. E. O'Maille, J. P. Noel, and R. M. Coates. 2007. Interception of the enzymatic conversion of farnesyl diphosphate to 5-epi-aristolochene by using a fluoro substrate analogue: 1-fluorogermacrene A from (2E,6Z)-6-fluorofarnesyl diphosphate. Chembiochem 8:1826-1833.
18. Gust, B., G. L. Challis, K. Fowler, T. Kieser, and K. F. Chater. 2003. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. USA 100:1541-1546.
19. Gutta, P., and D. J. Tantillo. 2005. Proton sandwiches: nonclassical carbocations with tetracoordinate protons. Angew Chem. Int. Ed. Engl. 44:2719-2723.
20. Gutta, P., and D. J. Tantillo. 2006. Theoretical studies on farnesyl cation cyclization: pathways to pentalenene. J. Am. Chem. Soc. 128:6172-6179.
21. Hamano, Y., T. Kuzuyama, N. Itoh, K. Furihata, H. Seto, and T. Dairi. 2002. Functional analysis of eubacterial diterpene cyclases responsible for biosynthesis of a diterpene antibiotic, terpentecin. J. Biol. Chem. 277:37098-37104.
22. He, W., J. Huang, X. Sun, and A. J. Frontier. 2008. Total synthesis of (+/-)-merrilactone A. J. Am. Chem. Soc. 130:300-308.
23. He, X., and D. E. Cane. 2004. Mechanism and stereochemistry of the germacradienol/germacrene D synthase of Streptomyces coelicolor A3(2). J. Am. Chem. Soc. 126:2678-2679.
24. Jenkins, C. M., I. Pikuleva, and M. R. Waterman. 1998. Expression of eukaryotic cytochromes P450 in E. coli. Methods Mol. Biol. 107:181-193.
25. Jenkins, C. M., and M. R. Waterman. 1998. NADPH-flavodoxin reductase and flavodoxin from Escherichia coli: characteristics as a soluble microsomal P450 reductase. Biochemistry 37:6106-6113.
26. Jiang, J., X. He, and D. E. Cane. 2007. Biosynthesis of the earthy odorant geosmin by a bifunctional Streptomyces coelicolor enzyme. Nat. Chem. Biol. 3:711-715.
27. Jiang, J., X. He, and D. E. Cane. 2006. Geosmin biosynthesis. Streptomyces coelicolor germacradienol/germacrene D synthase converts farnesyl diphosphate to geosmin. J. Am. Chem. Soc. 128:8128-8129.
28. Komatsu, M., M. Tsuda, S. Omura, H. Oikawa, and H. Ikeda. 2008. Identification and functional analysis of genes controlling biosynthesis of 2-methylisoborneol. Proc. Natl. Acad. Sci. USA 105:7422-7427.
29. Konig, W. A., N. Bulow, and Y. Saritas. 1999. Identification of sesquiterpene hydrocarbons by gas phase analytical methods. Flavour Fragrance J. 14:367-378.
30. Reference deleted.
31. Lawton, L. A., and G. A. Codd. 1991. Cyanobacterial (blue-green algal) toxins and thier significance in UK and European waters. J. Inst. Water Eng. Manag. 5:460-465.
32. Lesburg, C. A., G. Z. Zhai, D. E. Cane, and D. W. Christiansen. 1997. Crystal structure of pentalenene synthase: mechanistic insights on terpenoid cyclization reactions in biology. Science 277:1820-1824.
33. Lin, X., R. Hopson, and D. E. Cane. 2006. Genome mining in Streptomyces coelicolor: molecular cloning and characterization of a new sesquiterpene synthase. J. Am. Chem. Soc. 128:6022-6023.
34. Ludwig, F., A. Medger, H. Bornick, M. Opitz, K. Lang, M. Gottfert, and I. Roske. 2007. Identification and expression analyses of putative sesquiterpene synthase genes in Phormidium sp. and prevalence of geoA-like genes in a drinking water reservoir. Appl. Environ. Microbiol. 73:6988-6993.
35. Martin, V. J., D. J. Pitera, S. T. Withers, J. D. Newman, and J. D. Keasling. 2003. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat. Biotechnol. 21:796-802.
36. Munro, A. W., H. M. Girvan, and K. J. McLean. 2007. Cytochrome P450-redox partner fusion enzymes. Biochim. Biophys. Acta 1770:345-359.
37. + reductase, and cytochrome c. Arch. Biochem. Biophys. 321:229-238.
38. Naya, Y., G. D. Prestwich, and S. G. Spanton. 1982. Sesquiterpenes from termite soldiers: structure of amiteol, a new 5-beta, 7-beta, 10-beta-eudesmane from Amitermes excellens. Tetrahedron Lett. 23:3047-3050.
39. Picaud, S., M. E. Olsson, M. Brodelius, and P. E. Brodelius. 2006. Cloning, expression, purification and characterization of recombinant (+)-germacrene D synthase from Zingiber officinale. Arch. Biochem. Biophys. 452:17-28.
40. Ponec, R., P. Bultinck, P. Gutta, and D. J. Tantillo. 2006. Multicenter bonding in carbocations with tetracoordinate protons. J. Phys. Chem. A 110:3785-3789.
41. Prestwich, G. D., I. Abe, Y. F. Zheng, B. J. Robustell, and T. Y. Dang. 1999. Enzymatic cyclization of squalene analogs. Pure Appl. Chem. 71:1127-1131.
42. Prosser, I., A. L. Phillips, S. Gittings, M. J. Lewis, A. M. Hooper, J. A. Pickett, and M. H. Beale. 2002. (+)-(10R)-Germacrene A synthase from goldenrod, Solidago canadensis; cDNA isolation, bacterial expression and functional analysis. Phytochemistry 60:691-702.
43. Quaderer, R., S. Omura, H. Ikeda, and D. E. Cane. 2006. Pentalenolactone biosynthesis. Molecular cloning and assignment of biochemical function to PtlI, a cytochrome P450 of Streptomyces avermitilis. J. Am. Chem. Soc. 128:13036-13037.
44. Rynkiewicz, M. J., D. E. Cane, and D. W. Christiansen. 2001. Structure of trichodiene synthase from Fusarium sporotrichioides provides mechanistic inferences on the terpene cyclization cascade. Proc. Natl. Acad. Sci. USA 98:13543-13548.
45. Sambrook, J., and D. Russell. 2001. Molecular cloning: a labortory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Reference deleted.
47. Shishova, E. Y., L. Di Costanzo, D. E. Cane, and D. W. Christiansen. 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.
48. Svenning, M. M., T. Eriksson, and U. Rasmussen. 2005. Phylogeny of symbiotic cyanobacteria within the genus Nostoc based on 16S rDNA sequence analyses. Arch. Microbiol. 183:19-26.
49. Takahashi, S., and T. Koyama. 2006. Structure and function of cis-prenyl chain elongating enzymes. Chem. Rec. 6:194-205.
50. Takahashi, S., Y. Yeo, B. T. Greenhagen, T. McMullin, L. Song, J. Maurina-Brunker, R. Rossen, J. P. Noel, and J. Chappell. 2007. Metabolie engineering of sesquiterpene metabolism in yeast. Biotechnol. Bioeng. 97:170-181.
51. Tetzlaff, C. N., Z. You, D. E. Cane, S. Takamatsu, S. Omura, and H. Ikeda. 2006. A gene cluster for biosynthesis of the sesquiterpenoid antibiotic pentalenolactone in Streptomyces avermitilis. Biochemistry 45:6179-6186.
52. White, D. E., I. C. Stewart, R. H. Grubbs, and B. M. Stoltz. 2008. The catalytic asymmetric total synthesis of elatol. J. Am. Chem. Soc. 130:810-811.
53. Williams, P., K. Winzer, W. C. Chan, and M. Camara. 2007. Look who's talking: communication and quorum sensing in the bacterial world. Philos. Trans. R. Soc. Lond. B 362:1119-1134.
54. Woithe, K., N. Geib, K. Zerbe, D. B. Li, M. Heck, S. Fournier-Rousset, O. Meyer, F. Vitali, N. Matoba, K. Abou-Hadeed, and J. A. Robinson. 2007. Oxidative phenol coupling reactions catalyzed by OxyB: a cytochrome P450 from the vancomycin producing organism. Implications for vancomycin biosynthesis. J. Am. Chem. Soc. 129:6887-6895.
55. Zhao, B., X. Lin, L. Lei, D. C. Lamb, S. L. Kelly, M. R. Waterman, and D. E. Cane. 2008. Biosynthesis of the sesquiterpene antibiotic albaflavenonc in Streptomyces coelicolor A3(2). J. Biol. Chem. 283:8183-8189.