Skip to main content
Log in

Increased production of γ-lactones from hydroxy fatty acids by whole Waltomyces lipofer cells induced with oleic acid

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Among several fatty acids tested, oleic acid was selected as the most efficient inducer for the production of 4-hydroxydodecanoic acid, a metabolite of β-oxidation, by Waltomyces lipofer. Cells were induced by incubation for 12 h in a medium containing 10 g l−1 yeast extract, 10 g l−1 peptone, 5 g l−1 oleic acid, 1 g l−1 glucose, and 0.05 % (w/v) Tween 80. The optimal reaction conditions for the production of γ-lactones by induced cells were pH 6.5, 35 °C, 200 rpm, 0.71 M Tris, 60 g l−1 hydroxy fatty acid, and 20 g l−1 cells. Non-induced cells produced 38 g l−1 γ-dodecalactone from 60 g l−1 10-hydroxystearic acid after 30 h, with a conversion yield of 63 % (w/w) and a productivity of 1.3 g l−1 h−1 under the optimized conditions, whereas induced cells produced 51 g l−1 γ-dodecalactone from 60 g l−1 10-hydroxystearic acid after 30 h, with a conversion yield of 85 % (w/w) and a productivity of 1.7 g l−1 h−1. The conversion yield and productivity of induced cells were 22 % and 1.3-fold higher, respectively, than those of non-induced cells. Induced cells also produced 28 g l−1 γ-decalactone and 12 g l−1 γ-butyrolactone from 60 g l−1 12-hydroxystearic acid and 60 g l−1 10-hydroxydecanoic acid, respectively, after 30 h. The concentration, conversion yield, and productivity of γ-dodecalactone and γ-decalactone are the highest reported thus far. This is the first study on the biotechnological production of γ-butyrolactone.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aguedo M, Beney L, Wache Y, Belin JM (2003) Mechanisms underlying the toxicity of lactone aroma compounds towards the producing yeast cells. J Appl Microbiol 94:258–265

    Article  PubMed  CAS  Google Scholar 

  • Alchihab M, Destain J, Aguedo M, Majad L, Ghalfi H, Wathelet JP, Thonart P (2009) Production of γ-decalactone by a psychrophilic and a mesophilic strain of the yeast Rhodotorula aurantiaca. Appl Biochem Biotechnol 158:41–50

    Article  PubMed  CAS  Google Scholar 

  • An JU, Joo YC, Oh DK (2013) New biotransformation process for the production of the fragrance compound γ-dodecalactone from 10-hydroxystearate by permeabilized Waltomyces lipofer cells. Appl Environ Microbiol 79:2636–2641

    Article  PubMed  CAS  Google Scholar 

  • Carrau FM, Medina K, Farina L, Boido E, Henschke PA, Dellacassa E (2008) Production of fermentation aroma compounds by Saccharomyces cerevisiae wine yeasts: effects of yeast assimilable nitrogen on two model strains. FEMS Yeast Res 8:1196–1207

    Article  PubMed  CAS  Google Scholar 

  • Chen TC, Ju YH (2001) An improved fractional crystallization method for the enrichment of γ-linolenic acid in borage oil fatty acid. Ind Eng Chem Res 40:3781–3784

    Article  CAS  Google Scholar 

  • Dommes P, Dommes V, Kunau WH (1983) β-Oxidation in Candida tropicalis. Partial purification and biological function of an inducible 2,4-dienoyl coenzyme A reductase. J Biol Chem 258:10846–10852

    PubMed  CAS  Google Scholar 

  • Elss S, Preston C, Hertzig C, Heckel F, Richling E, Schreier P (2005) Aroma profiles of pineapple fruit (Ananas comosus [L.] Merr.) and pineapple products. Lwt-Food Sci Technol 38:263–274

    Article  CAS  Google Scholar 

  • Endrizzi A, Awade AC, Belin JM (1993) Presumptive involvement of methyl ricinoleate β-oxidation in the production of γ-decalactone by the yeast Pichia guilliermondii. FEMS Microbiol Lett 114:153–160

    CAS  Google Scholar 

  • Endrizzi A, Pagot Y, Le Clainche A, Nicaud JM, Belin JM (1996) Production of lactones and peroxisomal β-oxidation in yeasts. Crit Rev Biotechnol 16:301–329

    Article  PubMed  CAS  Google Scholar 

  • Farbood MI, Morris JA, Mclean LB (1998) Fermentation process for preparing 10-hydroxy-C18-carboxylic acid and γ-dodecalactone derivatives. European Patent 0578388

  • Farbood MI, Willis BJ, Ramsey NJ (1985) Production of γ-decalactone. U S Patent 4560656

  • Feron G, Dufosse L, Pierard E, Bonnarme P, Quere JL, Spinnler H (1996) Production, identification, and toxicity of γ-decalactone and 4-hydroxydecanoic acid from Sporidiobolus spp. Appl Environ Microbiol 62:2826–2831

    PubMed  CAS  Google Scholar 

  • Fickers P, Benetti PH, Wache Y, Marty A, Mauersberger S, Smit MS, Nicaud JM (2005) Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications. FEMS Yeast Res 5:527–543

    Article  PubMed  CAS  Google Scholar 

  • Gatfield I (1988) Production of flavor and aroma compounds by biotechnology. Crit Rev Biotechnol 42:110–122

    Google Scholar 

  • Han O, Han SR (1995) Process for production of C10 and/or C12 gamma-lactones from the corresponding C10 and/or C12 carboxylic acid by means of microbial biotransformation in the presence of mineral oil. United States Patent 5457036

  • Hara Y, Takahashi K (2002) A novel production of γ-butyrolactone catalyzed by homogeneous ruthenium complexes. Catal Surv Jpn 6:73–78

    Article  CAS  Google Scholar 

  • Joo YC, Seo ES, Kim YS, Kim KR, Park JB, Oh DK (2012) Production of 10-hydroxystearic acid from oleic acid by whole cells of recombinant Escherichia coli containing oleate hydratase from Stenotrophomonas maltophilia. J Biotechnol 158:17–23

    Article  PubMed  CAS  Google Scholar 

  • Kawamoto S, Nozaki C, Tanaka A, Fukui S (1978) Fatty acid β-oxidation system in microbodies of n-alkane-grown Candida tropicalis. Eur J Biochem 83:609–613

    Article  PubMed  CAS  Google Scholar 

  • Kondo A, Liu Y, Furuta M, Fujita Y, Matsumoto T, Fukuda H (2000) Preparation of high activity whole cell biocatalyst by permeabilization of recombinant flocculent yeast with alcohol. Enzyme Microb Technol 27:806–811

    Article  PubMed  CAS  Google Scholar 

  • Lalel HJD, Singh Z, Tan SC (2003) Aroma volatiles production during fruit ripening of ‘Kensington Pride’ mango. Postharvest Biol Technol 27:323–336

    Article  CAS  Google Scholar 

  • Lee SL, Chen HY, Chen WC, Chou CC (1998) Production of -decalactone from ricinoleic acid by immobilized cells of Sporidiobolus salmonicolor. Process Biochem 33:453–459

    Article  CAS  Google Scholar 

  • Maga JA (1976) Lactones in foods. CRC Crit Rev Food Sci Nutr 8:1–56

    PubMed  CAS  Google Scholar 

  • Nicaud JM, Belin JM, Pagot Y, Joran EA (1996) Bioconversion of substrate with microbe auxotrophic for specific compound in medium deficient in this compound. French Patent 2734843

  • Pagot Y, Le Clainche A, Nicaud JM, Wache Y, Belin JM (1998) Peroxisomal β-oxidation activities and γ-decalactone production by the yeast Yarrowia lipolytica. Appl Microbiol Biotechnol 49:295–300

    Article  PubMed  CAS  Google Scholar 

  • Rabenhorst J, Gatfield I (2002) Method of producing γ-decalactone using Yarrowia lipolytica strain HR 145 (DSM 12397). United States Patent 6451565

  • Romero-Guido C, Belo I, Ta TM, Cao-Hoang L, Alchihab M, Gomes N, Thonart P, Teixeira JA, Destain J, Wache Y (2011) Biochemistry of lactone formation in yeast and fungi and its utilisation for the production of flavour and fragrance compounds. Appl Microbiol Biotechnol 89:535–547

    Article  PubMed  CAS  Google Scholar 

  • Schöttler M, Boland W (1995) On the biosynthesis of γ-dodecanolactone in ripening fruits: flavor constituents from strawberries (Fragaria ananassa) and peaches (Prunus persica). Helv Chim Acta 78:847–856

    Article  Google Scholar 

  • Sulter GJ, Waterham HR, Goodman JM, Veenhuis M (1990) Proliferation and metabolic significance of peroxisomes in Candida boidinii during growth on D-alanine or oleic acid as the sole carbon source. Arch Microbiol 153:485–489

    Article  PubMed  CAS  Google Scholar 

  • Ta TM, Cao-Hoang L, Phan-Thi H, Tran HD, Souffou N, Gresti J, Marechal PA, Cavin JF, Wache Y (2010) New insights into the effect of medium-chain-length lactones on yeast membranes. Importance of the culture medium. Appl Microbiol Biotechnol 87:1089–1099

    Article  PubMed  CAS  Google Scholar 

  • Titorenko VI, Nicaud JM, Wang H, Chan H, Rachubinski RA (2002) Acyl-CoA oxidase is imported as a heteropentameric, cofactor-containing complex into peroxisomes of Yarrowia lipolytica. J Cell Biol 156:481–494

    Article  PubMed  CAS  Google Scholar 

  • Valenciano S, Lucas JR, Pedregosa A, Monistrol IF, Laborda F (1996) Induction of β-oxidation enzymes and microbody proliferation in Aspergillus nidulans. Arch Microbiol 166:336–341

    Article  PubMed  CAS  Google Scholar 

  • Veenhuis M, Mateblowski M, Kunau WH, Harder W (1987) Proliferation of microbodies in Saccharomyces cerevisiae. Yeast 3:77–84

    Article  PubMed  CAS  Google Scholar 

  • Vose J, Tighe T, Schwartz M, Buel E (2001) Detection of γ-butyrolactone (GBL) as a natural component in wine. J Forensic Sci 46:1164–1167

    PubMed  CAS  Google Scholar 

  • Wache Y, Aguedo M, Nicaud JM, Belin JM (2003) Catabolism of hydroxyacids and biotechnological production of lactones by Yarrowia lipolytica. Appl Microbiol Biotechnol 61:393–404

    PubMed  CAS  Google Scholar 

  • Wilson WA, Hawley SA, Hardie DG (1996) Glucose repression/derepression in budding yeast: SNF1 protein kinase is activated by phosphorylation under derepressing conditions, and this correlates with a high AMP:ATP ratio. Curr Biol 6:1426–1434

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by a grant (no. 112002–3) from the Bio-industry Technology Development Program, Ministry for Food, Agriculture, Forestry and Fisheries, Republic of Korea.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Deok-Kun Oh.

Rights and permissions

Reprints and permissions

About this article

Cite this article

An, JU., Oh, DK. Increased production of γ-lactones from hydroxy fatty acids by whole Waltomyces lipofer cells induced with oleic acid. Appl Microbiol Biotechnol 97, 8265–8272 (2013). https://doi.org/10.1007/s00253-013-5089-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-5089-1

Keywords

Navigation