Microbial production of farnesol (FOH): Current states and beyond

Process Biochemistry

Volumn 46, Issue 6, 2011, Pages 1221-1229

  Wang, Chonglong ^a   Kim, Jae Yean ^a   Choi, Eui Sung ^b   Kim, Seon Won ^a  

^a Gyeongsang National University   (South Korea)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Farnesol; FPP synthase; Metabolic engineering; Microbial production; Phosphatases

Indexed keywords

CHEMICAL SYNTHESIS; E. COLI; FARNESOL; FPP SYNTHASE; GROWING DEMAND; INDUSTRIAL MATERIALS; INTRINSIC PROPERTY; LOW-YIELD; METABOLIC ENGINEERING; MICROBIAL PRODUCTION; NATURAL SOURCES; RECENT PROGRESS; S.CEREVISIAE; SYNTHESIS PATHWAYS; SYNTHETIC BIOLOGY; SYSTEMS BIOLOGY;

BIOCHEMISTRY; ESCHERICHIA COLI; EXTRACTION; GENES; MICROORGANISMS; PHOSPHATASES; SYNTHESIS (CHEMICAL);

METABOLISM;

ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 79955573491     PISSN: 13595113     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.procbio.2011.02.020     Document Type: Review

References (91)

1. Muntendam R, Melillo E, Ryden A, Kayser O. Perspectives and limits of engineering the isoprenoid metabolism in heterologous hosts. Appl Microbiol Biotechnol 2009;84:1003-19.
2. Grace MH. Chemical composition and biological activity of the volatiles of Anthemis melampodina and Pluchea dioscoridis. Phytother Res 2002;16:183-5. (Pubitemid 34297465)
3. Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils-a review. Food Chem Toxicol 2008;46:446-75. (Pubitemid 350297552)
4. Lorek J, Poggeler S, Weide MR, Breves R, Bockmuhl DP. Influence of farnesol on the morphogenesis of Aspergillus niger. J Basic Microbiol 2008;48:99-103.
5. Correll CC, Ng L, Edwards PA. Identification of farnesol as the non-sterol derivative of mevalonic acid required for the accelerated degradation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase. J Biol Chem 1994;269:17390-3.
6. Hornby JM, Jensen EC, Lisec AD, Tasto JJ, Jahnke B, Shoemaker R, et al. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 2001;67:2982-92. (Pubitemid 33644762)
7. Nickerson KW, Atkin AL, Hornby JM. Quorum sensing in dimorphic fungi: farnesol and beyond. Appl Environ Microbiol 2006;72:3805-13. (Pubitemid 43894839)
8. Ramage G, Saville SP, Wickes BL, Lopez-Ribot JL. Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 2002;68:5459-63. (Pubitemid 35265681)
9. Scheper MA, Shirtliff ME, Meiller TF, Peters BM, Jabra-Rizk MA. Farnesol, a fungal quorum-sensing molecule triggers apoptosis in human oral squamous carcinoma cells. Neoplasia 2008;10:954-63.
10. Shirtliff ME, Krom BP, Meijering RA, Peters BM, Zhu J, Scheper MA, et al. Farnesol-induced apoptosis in Candida albicans. Antimicrob Agents Chemother 2009;53:2392-401.
11. Joo JH, Jetten AM. Molecular mechanisms involved in farnesol-induced apoptosis. Cancer Lett 2010;287:123-35.
12. Goldberg L, Haklai R, Bauer V, Heiss A, Kloog Y.Newderivatives of farnesylthiosalicylic acid (salirasib) for cancer treatment: farnesylthiosalicylamide inhibits tumor growth in nude mice models. J Med Chem 2009;52:197-205.
13. Fuel composition comprising farnesene and farnesane derivatives and method of making and using same. WO2008/045555.
14. Lee H, Finckbeiner S, Yu JS, Wiemer DF, Eisner T, Attygalle AB. Characterization of (E,E)-farnesol and its fatty acid esters from anal scent glands of nutria (Myocastor coypus) by gas chromatography-mass spectrometry and gas chromatography-infrared spectrometry. J Chromatogr A 2007;1165:136-43. (Pubitemid 47313413)
15. Yu JS, Kleckley TS, Wiemer DF. Synthesis of farnesol isomers via a modified Wittig procedure. Org Lett 2005;7:4803-6. (Pubitemid 41579867)
16. Rohdich F, Hecht S, Gartner K, Adam P, Krieger C, Amslinger S, et al. Studies on the nonmevalonate terpene biosynthetic pathway: metabolic role of IspH (LytB) protein. Proc Natl Acad Sci U S A 2002;99:1158-63. (Pubitemid 34136463)
17. Bloch K, Chaykin S, Phillips AH, De Waard A. Mevalonic acid pyrophosphate and isopentenylpyrophosphate. J Biol Chem 1959;234:2595-604.
18. Pitera DJ, Paddon CJ, Newman JD, Keasling JD. Balancing a heterologous mevalonate pathway for improved isoprenoid production in Escherichia coli. Metab Eng 2007;9:193-207. (Pubitemid 46329511)
19. Wang CW, Oh MK, Liao JC. Engineered isoprenoid pathway enhances astaxanthin production in Escherichia coli. Biotechnol Bioeng 1999;62:235-41. (Pubitemid 29001909)
20. Martin VJ, Pitera DJ, Withers ST, Newman JD, Keasling JD. Engineering amevalonate pathway in Escherichia coli for production of terpenoids. Nat Biotechnol 2003;21:796-802. (Pubitemid 36791399)
21. Polakowski T, Stahl U, Lang C. Overexpression of a cytosolic hydroxymethylglutaryl-CoA reductase leads to squalene accumulation in yeast. Appl Microbiol Biotechnol 1998;49:66-71. (Pubitemid 28055383)
22. Tsuruta H, Paddon CJ, Eng D, Lenihan JR, Horning T, Anthony LC, et al. High-level production of amorpha-4,11-diene, a precursor of the antimalarial agent artemisinin, in Escherichia coli. PLoS One 2009;4:e4489.
23. Faulkner A, Chen X, Rush J, Horazdovsky B, Waechter CJ, Carman GM, et al. The LPP1 and DPP1 gene products account for most of the isoprenoid phosphate phosphatase activities in Saccharomyces cerevisiae. J Biol Chem 1999;274:14831-7.
24. Song L. A soluble form of phosphatase in Saccharomyces cerevisiae capable of converting farnesyl diphosphate into E,E-farnesol. Appl Biochem Biotechnol 2006;128:149-58.
25. Cheng AX, Xiang CY, Li JX, Yang CQ, Hu WL, Wang LJ, et al. The rice (E)-beta-caryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. Phytochemistry 2007;68:1632-41.
26. Grochowski LL, Xu H, White RH. Methanocaldococcus jannaschii uses amodified mevalonate pathway for biosynthesis of isopentenyl diphosphate. J Bacteriol 2006;188:3192-8.
27. Hiser L, Basson ME, Rine J. ERG10 from Saccharomyces cerevisiae encodes acetoacetyl-CoA thiolase. J Biol Chem 1994;269:31383-9. (Pubitemid 24379490)
28. Stewart PR, Rudney H. The biosynthesis of beta-hydroxy-beta- methylglutaryl coenzyme A in yeast. 3. Purification and properties of the condensing enzyme thiolase system. J Biol Chem 1966;241:1212-21.
29. Basson ME, Thorsness M, Rine J. Saccharomyces cerevisiae contains two functional genes encoding 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Proc Natl Acad Sci U S A 1986;83:5563-7. (Pubitemid 16001260)
30. Hampton RY, Rine J. Regulated degradation of HMG-CoA reductase, an integral membrane protein of the endoplasmic reticulum, in yeast. J Cell Biol 1994;125:299-312. (Pubitemid 24135944)
31. Oulmouden A, Karst F. Isolation of the ERG12 gene of Saccharomyces cerevisiae encoding mevalonate kinase. Gene 1990;88:253-7. (Pubitemid 20170975)
32. Tsay YH, Robinson GW. Cloning and characterization of ERG8, an essential gene of Saccharomyces cerevisiae that encodes phosphomevalonate kinase. Mol Cell Biol 1991;11:620-31. (Pubitemid 21895410)
33. Cordier H, Lacombe C, Karst F, Berges T. The Saccharomyces cerevisiae mevalonate diphosphate decarboxylase (erg19p) forms homodimers in vivo, and a single substitution in a structurally conserved region impairs dimerization. Curr Microbiol 1999;38:290-4. (Pubitemid 29203166)
34. Anderson MS, Muehlbacher M, Street IP, Proffitt J, Poulter CD. Isopentenyl diphosphate:dimethylallyl diphosphate isomerase. An improved purification of the enzyme and isolation of the gene from Saccharomyces cerevisiae. J Biol Chem 1989;264:19169-75. (Pubitemid 19285827)
35. Mayer MP, Hahn FM, Stillman DJ, Poulter CD. Disruption and mapping of IDI1, the gene for isopentenyl diphosphate isomerase in Saccharomyces cerevisiae. Yeast 1992;8:743-8.
36. Xiang S, Usunow G, Lange G, Busch M, Tong L. Crystal structure of 1-deoxy-D-xylulose 5-phosphate synthase, a crucial enzyme for isoprenoids biosynthesis. J Biol Chem 2007;282:2676-82. (Pubitemid 47076757)
37. Hill RE, Spenser ID. Biosynthesis of vitamin B6: incorporation of three-carbon units. Science 1970;169:773-5.
38. Hill RE, Himmeldirk K, Kennedy IA, Pauloski RM, Sayer BG, Wolf E, et al. The biogenetic anatomy of vitamin B6. A 13CNMRinvestigation of the biosynthesis of pyridoxol in Escherichia coli. J Biol Chem 1996;271:30426-35.
39. Takahashi S, Kuzuyama T, Watanabe H, Seto H. A 1-deoxy-D-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-D-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proc Natl Acad Sci U S A 1998;95:9879-84. (Pubitemid 28415263)
40. Richard SB, Bowman ME, Kwiatkowski W, Kang I, Chow C, Lillo AM, et al. Structure of 4-diphosphocytidyl-2-C-methylerythritol synthetase involved in mevalonate-independent isoprenoid biosynthesis. Nat Struct Biol 2001;8:641-8. (Pubitemid 32613015)
41. Luttgen H, Rohdich F, Herz S, Wungsintaweekul J, Hecht S, Schuhr CA, et al. Biosynthesis of terpenoids: YchB protein of Escherichia coli phosphorylates the 2-hydroxy group of 4-diphosphocytidyl-2C-methyl-D-erythritol. Proc Natl Acad Sci U S A 2000;97:1062-7. (Pubitemid 30080812)
42. Herz S, Wungsintaweekul J, Schuhr CA, Hecht S, Luttgen H, Sagner S, et al. Biosynthesis of terpenoids: YgbB protein converts 4-diphosphocytidyl- 2C-methyl-D-erythritol 2-phosphate to 2C-methyl-D-erythritol 2,4-cyclodiphosphate. Proc Natl Acad Sci U S A 2000;97:2486-90. (Pubitemid 30159197)
43. Kemp LE, Bond CS, Hunter WN. Structure of 2C-methyl-d-erythritol 2,4- cyclodiphosphate synthase: an essential enzyme for isoprenoid biosynthesis and target for antimicrobial drug development. Proc Natl Acad Sci U S A 2002;99:6591-6. (Pubitemid 34526177)
44. Rohdich F, Bacher A, Eisenreich W. Perspectives in anti-infective drug design. The late steps in the biosynthesis of the universal terpenoid precursors, isopentenyl diphosphate and dimethylallyl diphosphate. Bioorg Chem 2004;32:292-308.
45. Campos N, Rodriguez-Concepcion M, Seemann M, Rohmer M, Boronat A. Identification of gcpE as a novel gene of the 2-C-methyl-D-erythritol 4- phosphate pathway for isoprenoid biosynthesis in Escherichia coli. FEBS Lett 2001;488:170-3. (Pubitemid 32103591)
46. Hahn FM, Hurlburt AP, Poulter CD. Escherichia coli open reading frame 696 is idi, a nonessential gene encoding isopentenyl diphosphate isomerase. J Bacteriol 1999;181:4499-504. (Pubitemid 29357928)
47. Schulbach MC, Brennan PJ, Crick DC. Identification of a short (C15) chain Z-isoprenyl diphosphate synthase and a homologous long (C50) chain isoprenyl diphosphate synthase in Mycobacterium tuberculosis. J Biol Chem 2000;275:22876-81.
48. Ambo T, Noike M, Kurokawa H, Koyama T. Cloning and functional analysis of novel short-chain cis-prenyltransferases. Biochem Biophys Res Commun 2008;375:536-40.
49. Sallaud C, Rontein D, Onillon S, Jabes F, Duffe P, Giacalone C, et al. A novel pathway for sesquiterpene biosynthesis from Z,Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites. Plant Cell 2009;21:301-17.
50. Klionsky DJ, Emr SD. Membrane protein sorting: biosynthesis, transport and processing of yeast vacuolar alkaline phosphatase. EMBO J 1989;8:2241-50.
51. Tokuhiro K, Muramatsu M, Ohto C, Kawaguchi T, Obata S, Muramoto N, et al. Overproduction of geranylgeraniol by metabolically engineered Saccharomyces cerevisiae. Appl Environ Microbiol 2009;75:5536-43.
52. Touze T, Blanot D, Mengin-Lecreulx D. Substrate specificity and membrane topology of Escherichia coli PgpB, an undecaprenyl pyrophosphate phosphatase. J Biol Chem 2008;283:16573-83.
53. Wang C, Yoon SH, Shah AA, Chung YR, Kim JY, Choi ES, et al. Farnesol production from Escherichia coli by harnessing the exogenous mevalonate pathway. Biotechnol Bioeng 2010;107:421-9.
54. Enayetallah AE, Grant DF. Effects of human soluble epoxide hydrolase polymorphisms on isoprenoid phosphate hydrolysis. Biochem Biophys Res Commun 2006;341:254-60. (Pubitemid 43117412)
55. Cao L, Zhang P, Grant DF. An insect farnesyl phosphatase homologous to the N-terminal domain of soluble epoxide hydrolase. Biochem Biophys Res Commun 2009;380:188-92.
56. Shlomai J, Kornberg A. Deoxyuridine triphosphatase of Escherichia coli. Purification, properties, and use as a reagent to reduce uracil incorporation into DNA. J Biol Chem 1978;253:3305-12. (Pubitemid 8338670)
57. Withers ST, Gottlieb SS, Lieu B, Newman JD, Keasling JD. Identification of isopentenol biosynthetic genes from Bacillus subtilis by a screening method based on isoprenoid precursor toxicity. Appl Environ Microbiol 2007;73:6277-83. (Pubitemid 47548039)
58. Degenhardt J, Kollner TG, Gershenzon J. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 2009;70:1621-37.
59. Schnee C, Kollner TG, Gershenzon J, Degenhardt J. The maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)- beta-farnesene, (E)-nerolidol, and (E,E)-farnesol after herbivore damage. Plant Physiol 2002;130:2049-60. (Pubitemid 36035200)
60. Rynkiewicz MJ, Cane DE, Christianson DW. Structure of trichodiene synthase from Fusarium sporotrichioides provides mechanistic inferences on the terpene cyclization cascade. Proc Natl Acad Sci U S A 2001;98:13543-8. (Pubitemid 33115934)
61. Hornby JM, Nickerson KW. Enhanced production of farnesol by Candida albicans treated with four azoles. Antimicrob Agents Chemother 2004;48:2305-7. (Pubitemid 38691638)
62. Hornby JM, Kebaara BW, Nickerson KW. Farnesol biosynthesis in Candida albicans: cellular response to sterol inhibition by zaragozic acid B. Antimicrob Agents Chemother 2003;47:2366-9. (Pubitemid 36753605)
63. Muramatsu M, Ohto C, Obata S, Sakuradani E, Shimizu S. Various oils and detergents enhance the microbial production of farnesol and related prenyl alcohols. J Biosci Bioeng 2008;106:263-7.
64. Langford ML, Hasim S, Nickerson KW, Atkin AL. Activity and toxicity of farnesol towards Candida albicans are dependent on growth conditions. Antimicrob Agents Chemother 2010;54:940-2.
65. Muramatsu M, Ohto C, Obata S, Sakuradani E, Shimizu S. Alkaline pH enhances farnesol production by Saccharomyces cerevisiae. J Biosci Bioeng 2009;108:52-5.
66. Serrano R, Ruiz A, Bernal D, Chambers JR, Arino J. The transcriptional response to alkaline pH in Saccharomyces cerevisiae: evidence for calcium-mediated signalling. Mol Microbiol 2002;46:1319-33.
67. Song L. Recovery of E,E-farnesol from cultures of yeast erg9 mutants: extraction with polymeric beads and purification by normal-phase chromatography. Biotechnol Prog 2009;25:1111-4.
68. Chambon C, Ladeveze V, Oulmouden A, Servouse M, Karst F. Isolation and properties of yeast mutants affected in farnesyl diphosphate synthetase. Curr Genet 1990;18:41-6. (Pubitemid 20233674)
69. Grabowska D, Karst F, Szkopinska A. Effect of squalene synthase gene disruption on synthesis of polyprenols in Saccharomyces cerevisiae. FEBS Lett 1998;434:406-8. (Pubitemid 29052265)
70. Asadollahi MA, Maury J, Moller K, Nielsen KF, Schalk M, Clark A, et al. Production of plant sesquiterpenes in Saccharomyces cerevisiae: effect of ERG9 repression on sesquiterpene biosynthesis. Biotechnol Bioeng 2008;99:666-77. (Pubitemid 351158264)
71. Paradise EM, Kirby J, Chan R, Keasling JD. Redirection of flux through the FPP branch-point in Saccharomyces cerevisiae by down-regulating squalene synthase. Biotechnol Bioeng 2008;100:371-8. (Pubitemid 351758178)
72. Asadollahi MA, Maury J, Patil KR, Schalk M, Clark A, Nielsen J. Enhancing sesquiterpene production in Saccharomyces cerevisiae through in silico driven metabolic engineering. Metab Eng 2009;11:328-34.
73. Takahashi S, Yeo Y, Greenhagen BT, McMullin T, Song L, Maurina-Brunker J, et al. Metabolic engineering of sesquiterpene metabolism in yeast. Biotechnol Bioeng 2007;97:170-81. (Pubitemid 46649764)
74. Ohto C, Muramatsu M, Obata S, Sakuradani E, Shimizu S. Overexpression of the gene encoding HMG-CoA reductase in Saccharomyces cerevisiae for production of prenyl alcohols. Appl Microbiol Biotechnol 2009;82:837-45.
75. DCV, INC. Bio-Technical Resources. Production of farnesol and geranylgeraniol. US2003/0092144A1.
76. Ohto C, Muramatsu M, Obata S, Sakuradani E, Shimizu S. Prenyl alcohol production by expression of exogenous isopentenyl diphosphate isomerase and farnesyl diphosphate synthase genes in Escherichia coli. Biosci Biotechnol Biochem 2009;73:186-8.
77. Muramatsu M, Ohto C, Obata S, Sakuradani E, Shimizu S. Accumulation of prenyl alcohols by terpenoid biosynthesis inhibitors in various microorganisms. Appl Microbiol Biotechnol 2008;80:589-95.
78. Sikkema J, de Bont JA, Poolman B. Mechanisms ofmembrane toxicity of hydrocarbons. Microbiol Rev 1995;59:201-22.
79. Derengowski LS, De-Souza-Silva C, Braz SV, Mello-De-Sousa TM, Bao SN, Kyaw CM, et al. Antimicrobial effect of farnesol, a Candida albicans quorum sensing molecule, on Paracoccidioides brasiliensis growth and morphogenesis. Ann Clin Microbiol Antimicrob 2009;8:13.
80. Jin YS, Stephanopoulos G. Multi-dimensional gene target search for improving lycopene biosynthesis in Escherichia coli. Metab Eng 2007;9:337-47. (Pubitemid 47102684)
81. Alper H, Stephanopoulos G. Global transcription machinery engineering: a new approach for improving cellular phenotype. Metab Eng 2007;9:258-67. (Pubitemid 46809525)
82. Okochi M, Kurimoto M, Shimizu K, Honda H. Increase of organic solvent tolerance by overexpression of manXYZ in Escherichia coli. Appl Microbiol Biotechnol 2007;73:1394-9. (Pubitemid 46089514)
83. Hirasawa T, Yoshikawa K, Nakakura Y, Nagahisa K, Furusawa C, Katakura Y, et al. Identification of target genes conferring ethanol stress tolerance to Saccharomyces cerevisiae based on DNA microarray data analysis. J Biotechnol 2007;131:34-44. (Pubitemid 47042927)
84. Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang RY, Algire MA, et al. Creation of a bacterial cell controlled by a chemically synthesized genome. Science 2010;329:52-6.
85. Forster AC, Church GM. Towards synthesis of a minimal cell. Mol Syst Biol 2006;2:45.
86. Gustafsson C, Govindarajan S, Minshull J. Codon bias and heterologous protein expression. Trends Biotechnol 2004;22:346-53. (Pubitemid 38887543)
87. Zhang K, Sawaya MR, Eisenberg DS, Liao JC. Expanding metabolism for biosynthesis of nonnatural alcohols. Proc Natl Acad Sci U S A 2008;105:20653-8.
88. Chemler JA, Fowler ZL, McHugh KP, Koffas MA. Improving NADPH availability for natural product biosynthesis in Escherichia coli by metabolic engineering. Metab Eng 2010;12:96-104.
89. Kizer L, Pitera DJ, Pfleger BF, Keasling JD. Application of functional genomics to pathway optimization for increased isoprenoid production. Appl Environ Microbiol 2008;74:3229-41. (Pubitemid 351747029)
90. Rutherford BJ, Dahl RH, Price RE, Szmidt HL, Benke PI, Mukhopadhyay A, et al. Functional genomic study of exogenous n-butanol stress in Escherichia coli. Appl Environ Microbiol 2010;76:1935-45.
91. Kharel Y, Zhang YW, Fujihashi M, Miki K, Koyama T. Identification of Significant residues for homoallylic substrate binding of Micrococcus luteus B-P 26 undecaprenyl diphosphate synthase. J Biol Chem 2001;276:28459-64.