A squalene synthase-like enzyme initiates production of tetraterpenoid hydrocarbons in Botryococcus braunii Race L

Nature Communications

Volumn 7, Issue , 2016, Pages

  Thapa, Hem R ^a   Naik, Mandar T ^a   Okada, Shigeru ^b,c   Takada, Kentaro ^b,c   Molnár, István ^d   Xu, Yuquan ^d,e   Devarenne, Timothy P ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d UNIVERSITY OF ARIZONA   (United States)

^e INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; ENZYME; ERGOSTEROL; GERANYLGERANYL PYROPHOSPHATE; HYDROCARBON; LYCOPAOCTAENE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SQUALENE; SQUALENE SYNTHASE; SQUALESTATIN; UNCLASSIFIED DRUG; ALGAL PROTEIN; ISOENZYME; ISOPRENOID PHOSPHATE; RECOMBINANT PROTEIN; TERPENE; TRITIUM;

BIOFUEL; ENZYME ACTIVITY; HYDROCARBON; MICROALGA; SUBSTRATE; TERPENE;

ARTICLE; BIOSYNTHESIS; BOTRYOCOCCUS BRAUNII; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; MASS FRAGMENTOGRAPHY; NONHUMAN; OZONOLYSIS; ANALOGS AND DERIVATIVES; BIOCATALYSIS; ENZYME ASSAY; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; GREEN ALGA; KINETICS; METABOLISM; MOLECULAR CLONING;

BOTRYOCOCCUS BRAUNII;

ALGAL PROTEINS; BIOCATALYSIS; CHLOROPHYTA; CLONING, MOLECULAR; DNA, COMPLEMENTARY; ENZYME ASSAYS; ESCHERICHIA COLI; FARNESYL-DIPHOSPHATE FARNESYLTRANSFERASE; GENE EXPRESSION; ISOENZYMES; KINETICS; POLYISOPRENYL PHOSPHATES; RECOMBINANT PROTEINS; SQUALENE; SUBSTRATE SPECIFICITY; TERPENES; TRITIUM;

EID: 84964341630     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11198     Document Type: Article

References (65)

1. Moody, J. W., McGinty, C. M. & Quinn, J. C. Global evaluation of biofuel potential from microalgae. Proc. Natl Acad. Sci. USA 111, 8691-8696 (2014).
2. Chisti, Y. Constraints to commercialization of algal fuels. J. Biotechnol. 167, 201-214 (2013).
3. Banerjee, A., Sharma, R., Chisti, Y. & Banerjee, U. C. Botryococcus braunii: a renewable source of hydrocarbons and other chemicals. Crit. Rev. Biotechnol. 22, 245-279 (2002).
4. Yoshida, M., Tanabe, Y., Yonezawa, N. & Watanabe, M. M. Energy innovation potential of oleaginous microalgae. Biofuels 3, 761-781 (2012).
5. Lee, S. Y., Kim, H. M. & Cheon, S. Metabolic engineering for the production of hydrocarbon fuels. Curr. Opin. Biotechnol. 33, 15-22 (2015).
6. Metzger, P. & Largeau, C. Botryococcus braunii: a rich source for hydrocarbons and related ether lipids. Appl. Microbiol. Biotechnol. 66, 486-496 (2005).
7. Hillen, L. W., Pollard, G., Wake, L. V. & White, N. Hydrocracking of the oils of Botryococcus braunii to transport fuels. Biotechnol. Bioeng. 24, 193-205 (1982).
8. Moldowan, J. M. & Seifert, W. K. First discovery of botryococcane in petroleum. J. Chem. Soc. Chem. Commun. 19, 912-914 (1980).
9. Mckirdy, D. M., Cox, R. E., Volkman, J. K. & Howell, V. J. Botryococcane in a new class of Australian non-marine crude oils. Nature 320, 57-59 (1986).
10. Lichtfouse, E., Derenne, S., Mariotti, A. & Largeau, C. Possible algal origin of long chain odd n-alkanes in immature sediments as revealed by distributions and carbon isotope ratios. Org. Geochem. 22, 1023-1027 (1994).
11. Glikson, M., Lindsay, K. & Saxby, J. Botryococcus-A planktonic green alga, the source of petroleum through the ages: transmission electron microscopical studies of oil shales and petroleum source rocks. Org. Geochem. 14, 14 (1989).
12. Adam, P., Schaeffer, P. & Albrecht, P. C40 monoaromatic lycopene derivatives as indicators of the contribution of the alga Botryococcus braunii race L to the organic matter of Messel oil shale (Eocene, Germany). Org. Geochem. 37, 584-596 (2006).
13. Khan, N. E., Nybo, E. S., Chappell, J. & Curtis, W. R. Triterpene hydrocarbon production engineered into a metabolically versatile host-Rhodobacter capsulatus. Biotechnol. Bioeng. 112, 1523-1532 (2015).
14. Rohmer, M. The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat. Prod. Rep. 16, 565-574 (1999).
15. Sato, Y., Ito, Y., Okada, S., Murakami, M. & Abe, H. Biosynthesis of the triterpenoids, botryococcenes and tetramethylsqualene in the B race of Botryococcus braunii via the non-mevalonate pathway. Tetrahedron Lett. 44, 7035-7037 (2003).
16. Metzger, P. & Casadevall, E. Lycopadiene, a tetraterpenoid hydrocarbon from new strains of the green-alga Botryococcus braunii. Tetrahedron Lett. 28, 3931-3934 (1987).
17. Robinson, G. W., Tsay, Y. H., Kienzle, B. K., Smith-Monroy, C. A. & Bishop, R. W. Conservation between human and fungal squalene synthetases: similarities in structure, function, and regulation. Mol. Cell. Biol. 13, 12 (1993).
18. Rohmer, M. Hopanoids. Handbook of Hydrocarbon and Lipid Microbiology 133-142 (Springer, 2010).
19. Poulter, C. D. Biosynthesis of non-head-to-tail terpenes-formation of 1-1 and 1-3 linkages. Acc. Chem. Res. 23, 70-77 (1990).
20. Metzger, P., Pouet, Y. & Summons, R. Chemtotaxonomic evidence for the similarity between Botryococcus braunii L race and Botryococcus neglectus. Phytochemistry 44, 1071-1075 (1997).
21. Zhang, Z., Metzger, P. & Sachs, J. P. Biomarker evidence for the co-occurrence of three races (A, B and L) of Botryococcus braunii in El Junco Lake, Galápagos. Org. Geochem. 38, 20 (2007).
22. Sato, T. et al. Sesquarterpenes (C35 terpenes) biosynthesized via the cyclization of a linear C35 isoprenoid by a tetraprenyl-beta-curcumene synthase and a tetraprenyl-beta-curcumene cyclase: identification of a new terpene cyclase. J. Am. Chem. Soc. 133, 9734-9737 (2011).
23. Okada, S., Devarenne, T. P., Murakami, M., Abe, H. & Chappell, J. Characterization of botryococcene synthase enzyme activity, a squalene synthase-like activity from the green microalga Botryococcus braunii, Race B. Arch. Biochem. Biophys. 422, 110-118 (2004).
24. Stamellos, K. D. et al. Subcellular localization of squalene synthase in rat hepatic cells. Biochemical and immunochemical evidence. J. Biol. Chem. 268, 12825-12836 (1993).
25. Okada, S., Devarenne, T. P. & Chappell, J. Molecular characterization of squalene synthase from the green microalga Botryococcus braunii, Race B. Arch. Biochem. Biophys. 373, 307-317 (2000).
26. Gu, P., Ishii, Y., Spencer, T. A. & Shechter, I. Function-structure studies and identification of three enzyme domains involved in the catalytic activity in rat hepatic squalene synthase. J. Biol. Chem. 273, 12515-12525 (1998).
27. Pandit, J. et al. Crystal structure of human squalene synthase. A key enzyme in cholesterol biosynthesis. J. Biol. Chem. 275, 30610-30617 (2000).
28. Liu, C. I., Jeng, W. Y., Chang, W. J., Ko, T. P. & Wang, A. H. Binding modes of zaragozic acid A to human squalene synthase and staphylococcal dehydrosqualene synthase. J. Biol. Chem. 287, 18750-18757 (2012).
29. Liu, C. I. et al. Structural insights into the catalytic mechanism of human squalene synthase. Acta Crystallogr. D 70, 231-241 (2014).
30. Beck, G. et al. Characterization of the GGPP synthase gene family in Arabidopsis thaliana. Plant Mol. Biol. 82, 393-416 (2013).
31. Ignea, C. et al. Efficient diterpene production in yeast by engineering Erg20p into a geranylgeranyl diphosphate synthase. Metab. Eng. 27, 65-75 (2015).
32. Qureshi, A. A., Barnes, F. J., Semmler, E. J. & Porter, J. W. Biosynthesis of prelycopersene pyrophosphate and lycopersene by squalene synthetase. J. Biol. Chem. 248, 2755-2767 (1973).
33. Barnes, F. J., Qureshi, A. A., Semmler, E. J. & Porter, J. W. Prelycopersene pyrophosphate and lycopersene. Intermediates in carotene biosynthesis. J. Biol. Chem. 248, 2768-2773 (1973).
34. Kushwaha, S. C. & Kates, M. Isolation and identification of bacteriorhodopsin and minor C40-carotenoids in Halobacterium cutirubrum. Biochim. Biophys. Acta 316, 235-243 (1973).
35. Gregonis, D. & Rilling, H. The stereochemistry of trans-phytoene synthesis. Some observations on lycopersene as a carotene precursor and a mechanism for the synthesis of cis- and trans-phytoene. Biochemistry 13, 1538-1542 (1974).
36. Kushwaha, S. C., Kates, M. & Porter, J.W. Enzymatic synthesis of C40 carotenes by cell-free preparation from Halobacterium cutirubrum. Can. J. Biochem. 54, 816-823 (1976).
37. Niehaus, T. D. et al. Identification of unique mechanisms for triterpene biosynthesis in Botryococcus braunii. Proc. Natl Acad. Sci. USA 108, 12260-12265 (2011).
38. Baxter, A. et al. Squalestatin 1, a potent inhibitor of squalene synthase, which lowers serum cholesterol in vivo. J. Biol. Chem. 267, 11705-11708 (1992).
39. Bergstrom, J. D. et al. Zaragozic Acids-a family of fungal metabolites that are picomolar competitive inhibitors of squalene synthase. Proc. Natl Acad. Sci. USA 90, 80-84 (1993).
40. Lindsey, S. & Harwood, H. J. Inhibition of mammalian squalene synthetaseactivity by zaragozic acid a is a result of competitive-inhibition followed by mechanism-based irreversible inactivation. J. Biol. Chem. 270, 9083-9096 (1995).
41. Umeno, D. & Arnold, F. H. A C35 carotenoid biosynthetic pathway. Appl. Environ. Microbiol. 69, 3573-3579 (2003).
42. Umeno, D. & Arnold, F. H. Evolution of a pathway to novel long-chain carotenoids. J. Bacteriol. 186, 1531-1536 (2004).
43. Tobias, A. V. & Arnold, F. H. Biosynthesis of novel carotenoid families based on unnatural carbon backbones: a model for diversification of natural product pathways. Biochim. Biophys. Acta 1761, 235-246 (2006).
44. Wieland, B. et al. Genetic and biochemical analyses of the biosynthesis of the yellow carotenoid 4,4-diaponeurosporene of Staphylococcus aureus. J. Bacteriol. 176, 7719-7726 (1994).
45. Ortiz de Montellano, P. R., Wei, J. S., Vinson, W. A., Castillo, R. & Boparai, A. S. Substrate selectivity of squalene synthetase. Biochemistry 16, 2680-2685 (1977).
46. Koyama, T., Ogura, K. & Seto, S. Substrate specificity of squalene synthetase. Biochim. Biophys. Acta 617, 218-224 (1980).
47. Jarstfer, M. B., Zhang, D. L. & Poulter, C. D. Recombinant squalene synthase. Synthesis of non-head-to-tail isoprenoids in the absence of NADPH. J. Am. Chem. Soc. 124, 8834-8845 (2002).
48. Blagg, B. S., Jarstfer, M. B., Rogers, D. H. & Poulter, C. D. Recombinant squalene synthase. A mechanism for the rearrangement of presqualene diphosphate to squalene. J. Am. Chem. Soc. 124, 8846-8853 (2002).
49. Zhang, D. L. & Poulter, C. D. Biosynthesis of non-head-to-tail isoprenoids- synthesis of 1-1-structures and 1-3-structures by recombinant yeast squalene synthase. J. Am. Chem. Soc. 117, 1641-1642 (1995).
50. Pan, J. J. et al. Biosynthesis of squalene from farnesyl diphosphate in bacteria: three steps catalyzed by three enzymes. ACS Cent. Sci. 1, 77-82 (2015).
51. Vining, L. C. Roles of secondary metabolites from microbes. Ciba Found. Symp. 171, 184-194 (1992).
52. Weiss, T. L. et al. Colony organization in the green alga Botryococcus braunii (Race B) is specified by a complex extracellular matrix. Eukaryot. Cell 11, 1424-1440 (2012).
53. Niehaus, T. D. et al. Functional identification of triterpene methyltransferases from Botryococcus braunii race B. J. Biol. Chem. 287, 8163-8173 (2012).
54. Manquin, B. P., Morgan, J. A., Ju, J., Muller-Spath, T. & Clark, D. S. Production of C35 isoprenoids depends on H2 availability during cultivation of the hyperthermophile Methanococcus jannaschii. Extremophiles 8, 13-21 (2004).
55. Cario, A., Grossi, V., Schaeffer, P. & Oger, P. M. Membrane homeoviscous adaptation in the piezo-hyperthermophilic archaeon Thermococcus barophilus. Front. Microbiol. 6, 1152 (2015).
56. Jorgensen, K. et al. Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr. Opin. Plant Biol. 8, 280-291 (2005).
57. Field, B. & Osbourn, A. E. Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science 320, 543-547 (2008).
58. Nutzmann, H. W. & Osbourn, A. Gene clustering in plant specialized metabolism. Curr. Opin. Biotechnol. 26, 91-99 (2014).
59. Chu, S. P. The influence of the mineral composition of the medium on the growth of planktonic algae: part I. Methods and culture media. J. Ecol. 30, 284-325 (1942).
60. Metzger, P., Allard, B., Casadevall, E., Berkaloff, C. & Coute, A. Structure and chemistry of a new chemical race of Botryococcus braunii (Chlorophyceae) that produces lycopadiene, a tetraterpenoid hydrocarbon. J. Phycol. 26, 258-266 (1990).
61. Weiss, T. L. et al. Raman spectroscopy analysis of botryococcene hydrocarbons from the green microalga Botryococcus braunii. J. Biol. Chem. 285, 32458-32466 (2010).
62. Molnar, I. et al. Bio-crude transcriptomics: gene discovery and metabolic network reconstruction for the biosynthesis of the terpenome of the hydrocarbon oil-producing green alga, Botryococcus braunii race B (Showa). BMC Genomics 13, 576 (2012).
63. Garrett, S. R., Morris, R. J. & OMaille, P. E. Steady-state kinetic characterization of sesquiterpene synthases by gas chromatography-mass spectroscopy. Methods Enzymol. 515, 3-19 (2012).
64. Zhuang, X. & Chappell, J. Building terpene production platforms in yeast. Biotechnol. Bioeng. 112, 1854-1864 (2015).
65. Zhuang, X. Engineering novel Terpene Production Platforms in the Yeast Saccharomyces cerevisae. Theses and Dissertations-Plant and Soil Sciences Paper 17, 1-189 (2013).