Abstract
Terpenes are a huge group of natural compounds characterised by their predominantly pleasant smell. They are built up by isoprene units in cyclic or acyclic form and can be functionalised by carbonyl, hydroxyl or carboxyl groups and by presence of additional carbon–carbon double bonds (terpenoids). Currently, much more than 10,000 terpenoid compounds are known, and many thereof are present in different iso- and stereoforms. Terpenoids are secondary metabolites and can have important biological functions in living organisms. In many cases, the biological functions of terpenoids are not known at all. Nevertheless, terpenoids are used in large quantities as perfumes and aroma compounds for food additives. Terpenoids can be also precursors and building blocks for synthesis of complex chiral compounds in chemical and pharmaceutical industry. Unfortunately, only few terpenoids are available in large quantities at reasonable costs. Therefore, characterisation of suited biocatalysts specific for terpenoid compounds and development of biotransformation processes of abundant terpenoids to commercially interesting derivates becomes more and more important. This minireview summarises knowledge on catabolic pathways and biotransformations of acyclic monoterpenes that have received only little attention. Terpenoids with 20 or more carbon atoms are not a subject of this study.
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References
Aguilar JA, Zavala AN, Diaz-Perez C, Cervantes C, Diaz-Perez AL, Campos-Garcia J (2006) The atu and liu clusters are involved in the catabolic pathways for acyclic monoterpenes and leucine in Pseudomonas aeruginosa. Appl Environ Microbiol 72:2070–2079
Aguilar JA, Diaz-Perez C, Diaz-Perez AL, Rodriguez-Zavala JS, Nikolau BJ, Campos-Garcia J (2008) Substrate specificity of the 3-methylcrotonyl coenzyme A (CoA) and geranyl-CoA carboxylases from Pseudomonas aeruginosa. J Bacteriol 190:4888–4893
Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475
Bhattacharya D, Sarma PM, Krishnan S, Mishra S, Lal B (2003) Evaluation of genetic diversity among Pseudomonas citronellolis strains isolated from oily sludge-contaminated sites. Appl Environ Microbiol 69:1435–1441
Bode HB, Zeeck A, Pluckhahn K, Jendrossek D (2000) Physiological and chemical investigations into microbial degradation of synthetic poly(cis-1,4-isoprene). Appl Environ Microbiol 66:3680–3685
Bode HB, Kerkhoff K, Jendrossek D (2001) Bacterial degradation of natural and synthetic rubber. Biomacromolecules 2:295–303
Cantwell SG, Lau EP, Watt DS, Fall RR (1978) Biodegradation of acyclic isoprenoids by Pseudomonas species. J Bacteriol 135:324–333
Carrau FM, Medina K, Boido E, Farina L, Gaggero C, Dellacassa E, Versini G, Henschke PA (2005) De novo synthesis of monoterpenes by Saccharomyces cerevisiae wine yeasts. FEMS Microbiol Lett 243:107–115
Chang MC, Keasling JD (2006) Production of isoprenoid pharmaceuticals by engineered microbes. Nat Chem Biol 2:674–681
Chatterjee T, Bhattacharyya DK (2001) Biotransformation of limonene by Pseudomonas putida. Appl Microbiol Biotechnol 55:541–546
Chattopadhyay A, Förster-Fromme K, Jendrossek D (2010) PQQ-dependent alcohol dehydrogenase (QEDH) of Pseudomonas aeruginosa is involved in catabolism of acyclic terpenes. J Basic Microbiol 50:119–124
Chavez-Aviles M, Diaz-Perez AL, Reyes-de la Cruz H, Campos-Garcia J (2009) The Pseudomonas aeruginosa liuE gene encodes the 3-hydroxy-3-methylglutaryl coenzyme A lyase, involved in leucine and acyclic terpene catabolism. FEMS Microbiol Lett 296:117–123
Chavez-Aviles M, Diaz-Perez AL, Campos-Garcia J (2010) The bifunctional role of LiuE from Pseudomonas aeruginosa, displays additionally HIHG-CoA lyase enzymatic activity. Mol Biol Rep 37:1787–1791
de Carvalho CC, da Fonseca MM (2006) Biotransformation of terpenes. Biotechnol Adv 24:134–142
Demyttenaere JC, del Carmen HM, De Kimpe N (2000) Biotransformation of geraniol, nerol and citral by sporulated surface cultures of Aspergillus niger and Penicillium sp. Phytochemistry 55:363–373
Demyttenaere JC, Vanoverschelde J, De Kimpe N (2004) Biotransformation of (R)-(+)- and (S)-(-)-citronellol by Aspergillus sp. and Penicillium sp., and the use of solid-phase microextraction for screening. J Chromatogr A 1027:137–146
Diaz-Perez AL, Zavala-Hernandez AN, Cervantes C, Campos-Garcia J (2004) The gnyRDBHAL cluster is involved in acyclic isoprenoid degradation in Pseudomonas aeruginosa. Appl Environ Microbiol 70:5102–5110
Diaz-Perez AL, Roman-Doval C, Diaz-Perez C, Cervantes C, Sosa-Aguirre CR, Lopez-Meza JE, Campos-Garcia J (2007) Identification of the aceA gene encoding isocitrate lyase required for the growth of Pseudomonas aeruginosa on acetate, acyclic terpenes and leucine. FEMS Microbiol Lett 269:309–316
Diehl A, von Wintzingerode F, Görisch H (1998) Quinoprotein ethanol dehydrogenase of Pseudomonas aeruginosa is a homodimer—sequence of the gene and deduced structural properties of the enzyme. Eur J Biochem 257:409–419
Duetz WA, Bouwmeester H, van Beilen JB, Witholt B (2003) Biotransformation of limonene by bacteria, fungi, yeasts, and plants. Appl Microbiol Biotechnol 61:269–277
Fall RR (1981) 3-Methylcrotonyl-CoA and geranyl-CoA carboxylases from Pseudomonas citronellolis. Methods Enzymol 71(Pt C):791–799
Fall RR, Hector ML (1977) Acyl-coenzyme A carboxylases. Homologous 3-methylcrotonyl-CoA and geranyl-CoA carboxylases from Pseudomonas citronellolis. Biochemistry 16:4000–4005
Fall RR, Brown JL, Schaeffer TL (1979) Enzyme recruitment allows the biodegradation of recalcitrant branched hydrocarbons by Pseudomonas citronellolis. Appl Environ Microbiol 38:715–722
Förster-Fromme K, Jendrossek D (2005) Malate:quinone oxidoreductase (MqoB) is required for growth on acetate and linear terpenes in Pseudomonas citronellolis. FEMS Microbiol Lett 246:25–31
Förster-Fromme K, Jendrossek D (2006) Identification and characterization of the acyclic terpene utilization gene cluster of Pseudomonas citronellolis. FEMS Microbiol Lett 264:220–225
Förster-Fromme K, Jendrossek D (2008a) Biochemical characterization of isovaleryl-CoA dehydrogenase (LiuA) of Pseudomonas aeruginosa and the importance of liu genes for a functional catabolic pathway of methyl-branched compounds. FEMS Microbiol Lett 286:78–84
Förster-Fromme K, Jendrossek D (2008) Biochemical characterization of isovaleryl-CoA dehydrogenase (LiuA) of Pseudomonas aeruginosa and the importance of liu genes for a functional catabolic pathway of methyl-branched compounds. FEMS Microbiol Lett
Förster-Fromme K, Höschle B, Mack C, Bott M, Armbruster W, Jendrossek D (2006) Identification of genes and proteins necessary for catabolism of acyclic terpenes and leucine/isovalerate in Pseudomonas aeruginosa. Appl Environ Microbiol 72:4819–4828
Förster-Fromme K, Chattopadhyay A, Jendrossek D (2008) Biochemical characterization of AtuD from Pseudomonas aeruginosa, the first member of a new subgroup of acyl-CoA dehydrogenases with specificity for citronellyl-CoA. Microbiology 154:789–796
Förster-Fromme K, Jendrossek D (2010) AtuR is a repressor of acyclic terpene utilisation (Atu) gene cluster expression and specifically binds to two 13 bp inverted repeat sequences of the atuA-atuR intergenic region, FEMS Microbiol Lett, in press
Guan X, Diez T, Prasad TK, Nikolau BJ, Wurtele ES (1999) Geranoyl-CoA carboxylase: a novel biotin-containing enzyme in plants. Arch Biochem Biophys 362:12–21
Hall M, Hauer B, Stürmer R, Kroutil W, Faber K (2006) Asymmetric whole-cell bioreduction of an α,β-unsaturated aldehyde (citral): competing prim-alcohol dehydrogenase and C-C lyase activities. Tetrahedron Asymmetr 17:3058–3062
Hammer KA, Carson CF, Riley TV (1999) Antimicrobial activity of essential oils and other plant extracts. J Appl Microbiol 86:985–990
Harder J, Probian C (1995) Microbial degradation of monoterpenes in the absence of molecular oxygen. Appl Environ Microbiol 61:3804–3808
Hector ML, Fall RR (1976) Evidence for distinct 3-methylcrotonyl-CoA and geranyl-CoA carboxylases in Pseudomonas citronellolis. Biochem Biophys Res Commun 71:746–753
Hector ML, Murphey-Waldorf MF, Giertych TB, Hickey MJ, Haggard AA (1993) Isolation and characterization of Pseudomonas aeruginosa mutants defective in the utilizatiion of the terpenoid citronellic acid. World J Microbiol Biotechnol 9:562–565
Heyen U, Harder J (2000) Geranic acid formation, an initial reaction of anaerobic monoterpene metabolism in denitrifying Alcaligenes defragrans. Appl Environ Microbiol 66:3004–3009
Höschle B, Jendrossek D (2005) Utilization of geraniol is dependent on molybdenum in Pseudomonas aeruginosa: evidence for different metabolic routes for oxidation of geraniol and citronellol. Microbiology 151:2277–2283
Höschle B, Gnau V, Jendrossek D (2005) Methylcrotonyl-CoA carboxylase and geranyl-CoA carboxylase are involved in leucine/isovalerate utilisation (Liu) and in acyclic terpenes utilisation (Atu) and are encoded by liuB/liuD and atuC/atuF in Pseudomonas aeruginosa. Microbiology 151:3649–3656
Hylemon PB, Harder J (1999) Biotransformation of monoterpenes, bile acids, and other isoprenoids in anaerobic ecosystems. FEMS Microbiol Rev 22:475–488
Ishida T (2005) Biotransformation of terpenoids by mammals, microorganisms, and plant-cultured cells. Chem Biodivers 2:569–590
Iurescia S, Marconi AM, Tofani D, Gambacorta A, Paternò A, Devirgiliis C, van der Werf MJ, Zennaro E (1999) Identification and sequencing of beta-myrcene catabolism genes from Pseudomonas sp. strain M1. Appl Environ Microbiol 65:2871–2876
Joglekar SS, Dhavlikar RS (1969) Microbial transformation of terpenoids. I. Identification of metabolites produced by a pseudomonad from citronellal and citral. Appl Microbiol 18:1084–1087
Kaspera R, Krings U, Pescheck M, Sell D, Schrader J, Berger RG (2005) Regio- and stereoselective fungal oxyfunctionalisation of limonenes. Z Naturforsch C 60:459–466
Keitel T, Diehl A, Knaute T, Stezowski JJ, Hohne W, Görisch H (2000) X-ray structure of the quinoprotein ethanol dehydrogenase from Pseudomonas aeruginosa: basis of substrate specificity. J Mol Biol 297:961–974
King A, Dickinson JR (2000) Biotransformation of monoterpene alcohols by Saccaromyces cerevisiae, Torulaspora delbrueckii and Kleuveromyces lactis. Yeast 16:499–506
King AJ, Dickinson JR (2003) Biotransformation of hop aroma terpenoids by ale and lager yeasts. FEMS Yeast Res 3:53–62
Lange BM, Rujan T, Martin W, Croteau R (2000) Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc Natl Acad Sci U S A 97:13172–13177
Madyastha KM, Renganathan V (1983) Bio-degradation of acetates of geraniol, nerol & citronellol by P. incognita: isolation & identification of metabolites. Indian J Biochem Biophys 20:136–140
Mars AE, Gorissen JP, van den Beld I, Eggink G (2001) Bioconversion of limonene to increased concentrations of perillic acid by Pseudomonas putida GS1 in a fed-batch reactor. Appl Microbiol Biotechnol 56:101–107
Martin VJ, Pitera DJ, Withers ST, Newman JD, Keasling JD (2003) Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat Biotechnol 21:796–802
Müller A, Hauer B, Rosche B (2007a) Asymmetric alkene reduction by yeast old yellow enzymes and by a novel Zymomonas mobilis reductase. Biotechnol Bioeng 98:22–29
Müller A, Stürmer R, Hauer B, Rosche B (2007b) Stereospecific alkene reduction: novel activity of old yellow enzymes. Angew Chem Int Ed Engl 46:3316–3318
Muntendam R, Melillo E, Ryden A, Kayser O (2009) Perspectives and limits of engineering the isoprenoid metabolism in heterologous hosts. Appl Microbiol Biotechnol 84:1003–1019
Noge K, Kato M, Mori N, Kataoka M, Tanaka C, Yamasue Y, Nishida R, Kuwahara Y (2008) Geraniol dehydrogenase, the key enzyme in biosynthesis of the alarm pheromone, from the astigmatid mite Carpoglyphus lactis (Acari: Carpoglyphidae). FEBS J 275:2807–2817
Onken J, Berger RG (1999) Biotransformation of citronellol by the basidiomycete Cystoderma carcharias in an aerated-membrane bioreactor. Appl Microbiol Biotechnol 51:158–163
Paduch R, Kandefer-Szerszen M, Trytek M, Fiedurek J (2007) Terpenes: substances useful in human healthcare. Arch Immunol Ther Exp (Warsz) 55:315–327
Ponzoni C, Gasparetti C, Goretti M, Turchetti B, Pagnoni UM, Cramarossa MR, Fort L, Buzzini P (2008) Biotransformation of acyclic monoterpenoids by Debaryomyces sp., Kluyveromyces sp., and Pichia sp. strains of environmental origin. Chem Biodivers 5:471–483
Prakash O, Kumari K, Lal R (2007) Pseudomonas delhiensis sp. nov., from a fly ash dumping site of a thermal power plant. Int J Syst Evol Microbiol 57:527–531
Romero P, Karp P (2003) PseudoCyc, a pathway-genome database for Pseudomonas aeruginosa. J Mol Microbiol Biotechnol 5:230–239
Rose K, Steinbüchel A (2005) Biodegradation of natural rubber and related compounds: recent insights into a hardly understood catabolic capability of microorganisms. Appl Environ Microbiol 71:2803–2812
Rupp M, Görisch H (1988) Purification, crystallisation and characterization of quinoprotein ethanol dehydrogenase from Pseudomonas aeruginosa. Biol Chem Hoppe Seyler 369:431–439
Santos PM, Sa-Correia I (2009) Adaptation to beta-myrcene catabolism in Pseudomonas sp. M1: an expression proteomics analysis. Proteomics 9:5101–5111
Seubert W (1960) Degradation of isoprenoid compounds by microorganisms. I. Isolation and characterization of an isoprenoid-degrading bacterium, Pseudomonas citronellolis n. sp. J Bacteriol 79:426–434
Seubert W, Fass E (1964a) Studies on the bacterial degradation of isoprenoids. Iv. The purification and properties of beta-isohexenylglutaconyl-CoA-hydratase and beta-hydroxy-beta-isohexenylglutaryl-CoA-lyase. Biochem Z 341:23–34
Seubert W, Fass E (1964b) Studies on the bacterial degradation of isoprenoids.V. The mechanism of isoprenoid degradation. Biochem Z 341:35–44
Seubert W, Remberger U (1963) Studies on the bacterial degradation of isoprenoids. Ii. The role of carbon dioxide. Biochem Z 338:245–264
Seubert W, Fass E, Remberger U (1963) Studies on the bacterial degradation of isoprenoids. Iii. Purification and properties of geranyl carboxylase. Biochem Z 338:265–275
Speelmans G, Bijlsma A, Eggink G (1998) Limonene bioconversion to high concentrations of a single and stable product, perillic acid, by a solvent-resistant Pseudomonas putida strain. Appl Microbiol Biotechnol 50:538–544
Thompson ML, Marriott R, Dowle A, Grogan G (2010) Biotransformation of beta-myrcene to geraniol by a strain of Rhodococcus erythropolis isolated by selective enrichment from hop plants. Appl Microbiol Biotechnol 85:721–730
Tozoni D, Zacaria J, Vanderlinde R, Longaray Delamare AP, Echeverrigaray S (2010) Degradation of citronellol, citronellal and citronellyl acetate by Pseudomonas mendocina IBPse 105. Electr J Biotechnol 13
Trudgill PW (1990) Microbial metabolism of monoterpenes—recent developments. Biodegradation 1:93–105
van Beilen JB, Holtackers R, Luscher D, Bauer U, Witholt B, Duetz WA (2005) Biocatalytic production of perillyl alcohol from limonene by using a novel Mycobacterium sp. cytochrome P450 alkane hydroxylase expressed in Pseudomonas putida. Appl Environ Microbiol 71:1737–1744
Vandenbergh PA (1986) Bacterial method and compositions for isoprenoid degradation. United States Patent 4,593,003:1–12
Vandenbergh PA, Cole RL (1986) Plasmid involvement in linalool metabolism by Pseudomonas fluorescens. Appl Environ Microbiol 52:939–940
Vandenbergh PA, Wright AM (1983) Plasmid involvement in acyclic isoprenoid metabolism by Pseudomonas putida. Appl Environ Microbiol 45:1953–1955
van der Werf MJ, de Bont JA, Leak DJ (1997) Opportunities in microbial biotransformation of monoterpenes. Adv Biochem Eng Biotechnol 55:147–177
Wolken WA, van der Werf MJ (2001) Geraniol biotransformation-pathway in spores of Penicillium digitatum. Appl Microbiol Biotechnol 57:731–737
Wolken WA, Van Loo WJ, Tramper J, Van Der Werf MJ (2002) A novel, inducible, citral lyase purified from spores of Penicillium digitatum. Eur J Biochem 269:5903–5910
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This work was supported by a grant of the Deutsche Forschungsgemeinschaft to D.J.
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Fig. 1
Western blot analysis of proteins after SDS-PAGE for biotin-containing proteins. Samples are from P. aeruginosa PAO1 wild type (a), insertion mutant in liuD (b) or in atuR (c; modified from Förster-Fromme et al. 2008). Note, constitutive expression of AtuF in atuR mutant (c) (JPEG 67.7 kb)
Table 1
Vmax and KM values of P. aeruginosa acyl-CoA dehydrogenases (DOC 36 kb)
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Förster-Fromme, K., Jendrossek, D. Catabolism of citronellol and related acyclic terpenoids in pseudomonads. Appl Microbiol Biotechnol 87, 859–869 (2010). https://doi.org/10.1007/s00253-010-2644-x
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DOI: https://doi.org/10.1007/s00253-010-2644-x