Skip to main content
Log in

Catabolism of citronellol and related acyclic terpenoids in pseudomonads

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—a review. Food Chem Toxicol 46:446–475

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bode HB, Kerkhoff K, Jendrossek D (2001) Bacterial degradation of natural and synthetic rubber. Biomacromolecules 2:295–303

    Article  CAS  Google Scholar 

  • Cantwell SG, Lau EP, Watt DS, Fall RR (1978) Biodegradation of acyclic isoprenoids by Pseudomonas species. J Bacteriol 135:324–333

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chang MC, Keasling JD (2006) Production of isoprenoid pharmaceuticals by engineered microbes. Nat Chem Biol 2:674–681

    Article  CAS  Google Scholar 

  • Chatterjee T, Bhattacharyya DK (2001) Biotransformation of limonene by Pseudomonas putida. Appl Microbiol Biotechnol 55:541–546

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • de Carvalho CC, da Fonseca MM (2006) Biotransformation of terpenes. Biotechnol Adv 24:134–142

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Fall RR (1981) 3-Methylcrotonyl-CoA and geranyl-CoA carboxylases from Pseudomonas citronellolis. Methods Enzymol 71(Pt C):791–799

    Article  CAS  Google Scholar 

  • Fall RR, Hector ML (1977) Acyl-coenzyme A carboxylases. Homologous 3-methylcrotonyl-CoA and geranyl-CoA carboxylases from Pseudomonas citronellolis. Biochemistry 16:4000–4005

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hammer KA, Carson CF, Riley TV (1999) Antimicrobial activity of essential oils and other plant extracts. J Appl Microbiol 86:985–990

    Article  CAS  Google Scholar 

  • Harder J, Probian C (1995) Microbial degradation of monoterpenes in the absence of molecular oxygen. Appl Environ Microbiol 61:3804–3808

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hylemon PB, Harder J (1999) Biotransformation of monoterpenes, bile acids, and other isoprenoids in anaerobic ecosystems. FEMS Microbiol Rev 22:475–488

    Article  Google Scholar 

  • Ishida T (2005) Biotransformation of terpenoids by mammals, microorganisms, and plant-cultured cells. Chem Biodivers 2:569–590

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • King A, Dickinson JR (2000) Biotransformation of monoterpene alcohols by Saccaromyces cerevisiae, Torulaspora delbrueckii and Kleuveromyces lactis. Yeast 16:499–506

    Article  CAS  Google Scholar 

  • King AJ, Dickinson JR (2003) Biotransformation of hop aroma terpenoids by ale and lager yeasts. FEMS Yeast Res 3:53–62

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Onken J, Berger RG (1999) Biotransformation of citronellol by the basidiomycete Cystoderma carcharias in an aerated-membrane bioreactor. Appl Microbiol Biotechnol 51:158–163

    Article  CAS  Google Scholar 

  • Paduch R, Kandefer-Szerszen M, Trytek M, Fiedurek J (2007) Terpenes: substances useful in human healthcare. Arch Immunol Ther Exp (Warsz) 55:315–327

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Romero P, Karp P (2003) PseudoCyc, a pathway-genome database for Pseudomonas aeruginosa. J Mol Microbiol Biotechnol 5:230–239

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Rupp M, Görisch H (1988) Purification, crystallisation and characterization of quinoprotein ethanol dehydrogenase from Pseudomonas aeruginosa. Biol Chem Hoppe Seyler 369:431–439

    CAS  Google Scholar 

  • Santos PM, Sa-Correia I (2009) Adaptation to beta-myrcene catabolism in Pseudomonas sp. M1: an expression proteomics analysis. Proteomics 9:5101–5111

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Seubert W, Fass E (1964b) Studies on the bacterial degradation of isoprenoids.V. The mechanism of isoprenoid degradation. Biochem Z 341:35–44

    CAS  Google Scholar 

  • Seubert W, Remberger U (1963) Studies on the bacterial degradation of isoprenoids. Ii. The role of carbon dioxide. Biochem Z 338:245–264

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vandenbergh PA (1986) Bacterial method and compositions for isoprenoid degradation. United States Patent 4,593,003:1–12

    Google Scholar 

  • Vandenbergh PA, Cole RL (1986) Plasmid involvement in linalool metabolism by Pseudomonas fluorescens. Appl Environ Microbiol 52:939–940

    CAS  Google Scholar 

  • Vandenbergh PA, Wright AM (1983) Plasmid involvement in acyclic isoprenoid metabolism by Pseudomonas putida. Appl Environ Microbiol 45:1953–1955

    CAS  Google Scholar 

  • van der Werf MJ, de Bont JA, Leak DJ (1997) Opportunities in microbial biotransformation of monoterpenes. Adv Biochem Eng Biotechnol 55:147–177

    Google Scholar 

  • Wolken WA, van der Werf MJ (2001) Geraniol biotransformation-pathway in spores of Penicillium digitatum. Appl Microbiol Biotechnol 57:731–737

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant of the Deutsche Forschungsgemeinschaft to D.J.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dieter Jendrossek.

Electronic supplementary material

Below is the link to the electronic supplementary material.

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)

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-010-2644-x

Keywords

Navigation