Skip to main content
Log in

Bioflavour production from orange peel hydrolysate using immobilized Saccharomyces cerevisiae

  • Biotechnological products and process engineering
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The rising trend of bioflavour synthesis by microorganisms is hindered by the high manufacturing costs, partially attributed to the cost of the starting material. To overcome this limitation, in the present study, dilute-acid hydrolysate of orange peel was employed as a low-cost, rich in fermentable sugars substrate for the production of flavour-active compounds by Saccharomyces cerevisiae. With this purpose, the use of immobilized cell technology to protect cells against the various inhibitory compounds present in the hydrolysate was evaluated with regard to yeast viability, carbon and nitrogen consumption and cell ability to produce flavour active compounds. For cell immobilization the encapsulation in Ca alginate beads was used. The results were compared with those obtained using free-cell system. Based on the data obtained immobilized cells showed better growth performance and increased ability for de novo synthesis of volatile esters of "fruity" aroma (phenylethyl acetate, ethyl hexanoate, octanoate, decanoate and dodecanoate) than those of free cells. The potential for in situ production of new formulations containing flavour-active compounds derive from yeast cells and also from essential oil of orange peel (limonene, α-terpineol) was demonstrated by the fact that bioflavour mixture was found to accumulate within the beads. Furthermore, the ability of the immobilized yeast to perform efficiently repeated batch fermentations of orange peel hydrolysate for bioflavour production was successfully maintained after six consecutive cycles of a total period of 240 h.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alriksson B (2006) Ethanol from lignocellulose: alkali detoxification of dilute-acid spruce hydrolysates. Licentiate thesis, Faculty of Technology and Science Biochemistry. Karlstad University Studies, Sweden

    Google Scholar 

  • Belletti N, Ndagijimana M, Sisto C, Guerzoni ME, Lanciotti R, Gardini F (2004) Evaluation of the antimicrobial activity of citrus essences on Saccharomyces cerevisiae. J Agric Food Chem 52:6932–6938

    PubMed  CAS  Google Scholar 

  • Díaz-Montaño DM, Délia ML, Estarrón-Espinosa M, Strehaiano P (2008) Fermentative capability and aroma compound production by yeast strains isolated from Agave tequilana Weber juice. Enzyme Microb Technol 42:608–616

    Google Scholar 

  • Dubal SA, Tilkari YP, Momin SA, Borkar IV (2008) Biotechnological routes in flavour industries. Adv Biotechnol 3:20–30

    Google Scholar 

  • EU Regulation No 1334 (2008) Official J EU 354/34

  • Fan G, Lu W, Yao X, Zhang Y, Wang K, Pan S (2009) Effect of fermentation on free and bound volatile compounds of orange juice. Flav Fragrance J 24:219–225

    CAS  Google Scholar 

  • Furukawa K, Yamada T, Mizoguchi H, Hara S (2003) Increased ethyl caproate production by inositol limitation in Saccharomyces cerevisiae. J Biosci Bioeng 95:448–454

    PubMed  CAS  Google Scholar 

  • Kaur P, Kunze G, Satyanarayana T (2007) Yeast phytases: present scenario and future perspectives. Crit Rev Biotechnol 27:93–109

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Legras JL, Erny C, Le Jeune C, Lollie M, Adolphe Y, Demuyter C, Delobel P, Blondin B, Karst F (2010) Activation of two different resistance mechanisms in Saccharomyces cerevisiae upon exposure to octanoic and decanoic acids. Appl Environ Microbiol 76:7526–7535

    PubMed  CAS  Google Scholar 

  • Liu J, Zhu Y, Du G, Zhou J, Chen J (2013) Response of Saccharomyces cerevisiae to d-limonene-induced oxidative stress. Appl Microbiol Biotechnol. doi:10.1007/s00253-013-4931-9

    Google Scholar 

  • Lohrasbi M, Pourbafrani M, Niklasson C, Taherzadeh MJ (2010) Process design and economic analysis of a citrus waste biorefinery with biofuels and limonene as products. Bioresour Technol 101:7382–7388

    PubMed  CAS  Google Scholar 

  • Longo MA, Sanromán MA (2006) Production of food aroma compounds: microbial and enzymatic methodologies. Food Technol Biotechnol 44:335–353

    CAS  Google Scholar 

  • Luttrell B (1993) The biological relevance of the binding of calcium ions by inositol phosphates. J Biol Chem 268:1521–1524

    PubMed  CAS  Google Scholar 

  • Mallouchos A, Komaitis M, Koutinas A, Kanellaki M (2002) Investigation of volatiles evolution during the alcoholic fermentation of grape must using free and immobilized cells with the help of solid phase miroextraction (SPME) headspace sampling. J Agric Food Chem 50:3840–3848

    PubMed  CAS  Google Scholar 

  • Manojlovic V, Djonlagic J, Obradovic B, Nedovic V, Bugarski B (2006) Investigations of cell immobilization in alginate: rheological and electrostatic extrusion studies. J Chem Technol and Biotechnol 81:505–510

    CAS  Google Scholar 

  • Mantzouridou F, Paraskevopoulou A (2012) Volatile bio-ester production from orange pulp-containing medium using Saccharomyces cerevisiae. Food Bioprocess Technol. doi:10.1007/s11947-012-1009-0

    Google Scholar 

  • Mantzouridou F, Tsimidou MZ, Roukas T (2006) Performance of crude olive pomace oil and soybean oil during carotenoid production by Blakeslea trispora in submerged fermentation. J Agric Food Chem 54:2575–2581

    PubMed  CAS  Google Scholar 

  • Margaritis A, Kilonzo PM (2005) Production of ethanol using immobilised cell bioreactor systems. In: Nedović V, Willaert R (eds) Applications of cell immobilisation biotechnology. Springer, Netherlands, pp 375–405

    Google Scholar 

  • Mittal A, Singh G, Goyal V, Yadav A, Aggarwal NK (2012) Production of phytase by acido-thermophilic strain of Klebsiella sp. DB-3FJ711774.1 using orange peel flour under submerged fermentation. Innov Rom Food Biotechnol 10:18–27

    CAS  Google Scholar 

  • Natural colors and flavors market by types, applications and geography: global trends and forecasts, 2011–2016. Available at: www.marketsandmarkets.com/Market-Reports/natural-colors-flavors-market-676.html. Accessed May 2012

  • Nedovic V, Obradovic B, Leskošek-Cukalovic I, Trifunovic O, Pešic R, Bugarski B (2001) Electrostatic generation of alginate microbeads loaded with brewing yeast. Process Biochem 37:17–22

    CAS  Google Scholar 

  • Nedovic VA, Manojlovic V, Bugarski B, Willaert R (2010) State of the art in immobilized/encapsulated cell technology in fermentation processes. In: Encapsulation technologies for active food Ingredients and food processing. Springer, London, pp 119–146

    Google Scholar 

  • Oberoi HS, Vadlani PV, Madl RL, Saida L, Abeykoon JP (2010) Ethanol production from orange peels: two-stage hydrolysis and fermentation studies using optimized parameters through experimental design. J Agric Food Chem 58:3422–3429

    PubMed  CAS  Google Scholar 

  • Perkin WH Jr (1904) Experiments on the synthesis of the terpenes: Part I. Synthesis of terpin, inactive terpineol, and diterpene. J Chem Soc 85:656–671

    Google Scholar 

  • Pourbafrani M, Talebnia F, Niklasson C, Taherzadeh MJ (2007) Protective effect of encapsulation in fermentation of limonene-contained media and orange peel hydrolyzate. Int J Mol Sci 8:777–787

    CAS  Google Scholar 

  • Purwadi R, Taherzadeh MJ (2008) The performance of serial bioreactors in rapid continuous production of ethanol from dilute-acid hydrolyzates using immobilized cells. Biores Technol 99:2226–2233

    CAS  Google Scholar 

  • Rakin M, Mojovic L, Nikolic S, Vukasinovic M, Nedovic V (2009) Bioethanol production by immobilized Sacharomyces cerevisiae var. ellipsoideus cells. Afr J Biotechnol 8:464–471

    CAS  Google Scholar 

  • Rojas V, Gil JV, Piñaga F, Manzanares P (2001) Studies on acetate ester production by non-Saccharomyces wine yeasts. Int J Food Microbiol 70:283–289

    PubMed  CAS  Google Scholar 

  • Rossi SC, Vandenberghe LPS, Pereira BMP, Gago FD, Rizzolo JA, Pandey A (2009) Improving fruity aroma production by fungi in SSF using citric pulp. Food Res Int 42:484–486

    CAS  Google Scholar 

  • Saerens SM, Delvaux F, Verstrepen KJ, Van Dijck P, Thevelein JM, Delvaux FR (2008) Parameters affecting ethyl ester production by Saccharomyces cerevisiae during fermentation. Appl Environ Microbiol 74:454–461

    PubMed  CAS  Google Scholar 

  • Saerens SM, Delvaux FR, Verstrepen KJ, Thevelein JM (2010) Production and biological function of volatile esters in Saccharomyces cerevisiae. Microb Technol 3:165–177

    CAS  Google Scholar 

  • Schrader J (2007) Microbial flavour production. In: Berger RG (ed) Flavours and fragrances – chemistry, bioprocessing and sustainability. Springer, Heidelberg, pp 507–574

    Google Scholar 

  • Shen HY, Moonjai N, Verstrepen KJ, Delvaux F, Delvaux FR (2003a) Immobilization of Saccharomyces cerevisiae induces changes in the gene expression levels of HSP12, SSA3 and ATF1 during beer fermentation. J Am Soc Brew Chem 61:175–181

    CAS  Google Scholar 

  • Shen HY, Moonjai N, Verstrepen KJ, Delvaux F, Delvaux FR (2003b) Impact of attachment immobilization on yeast physiology and fermentation performance. J Am Soc Brew Chem 61:79–87

    CAS  Google Scholar 

  • Swiegers JH, Bartowsky EJ, Henschke PA, Pretorius IS (2005) Yeast and bacterial modulation of wine aroma and flavour. Aust J Grape Wine Res 11:139–173

    CAS  Google Scholar 

  • Taherzadeh MJ, Karimi K (2007) Acid-based hydrolysis processes for ethanol from lignocellulosic materials: a review. Biogeosciences 2:472–499

    CAS  Google Scholar 

  • Talebnia F, Taherzadeh MJ (2006) In situ detoxification and continuous cultivation of dilute-acid hydrolyzate to ethanol by encapsulated S. cerevisiae. J Biotechnol 125:377–384

    PubMed  CAS  Google Scholar 

  • Tataridis P, Ntagas P, Voulgaris I, Nerantzis ET (2005) Production of sparkling wine with immobilized yeast fermentation. Electron J Sci Technol 1:1–21

    Google Scholar 

  • Van Iersel MFM, Brouwer PE, Rombouts FM, Abee T (1999) Influence of yeast immobilization on fermentation and aldehyde reduction during the production of alcohol free beer. Enzyme Microb Tech 26:602–607

    Google Scholar 

  • Vilela A, Schuller D, Mendes-Faia A, Côrte-Real M (2013) Reduction of volatile acidity of acidic wines by immobilized Saccharomyces cerevisiae cells. Appl Microbiol Biotechnol 97:4991–5000

    PubMed  CAS  Google Scholar 

  • Westman JO, Ylitervo P, Franzén CJ, Taherzadeh MJ (2012) Effects of encapsulation of microorganisms on product formation during microbial fermentations. Appl Microbiol Biotechnol 96:1441–1454

    PubMed  CAS  Google Scholar 

  • Wilkins MR, Widmer WW, Grohmann KL (2007) Simultaneous saccharification and fermentation of citrus peel waste by Saccharomyces cerevisiae to produce ethanol. Process Biochem 42:1614–1619

    CAS  Google Scholar 

  • Willaert R, Nedovic VA (2006) Primary beer fermentation by immobilised yeast—a review on flavour formation and control strategies. J Chem Technol Biotechnol 81:1353–1367

    CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by BIOFLAVOUR, COST Action FA0907 (www.bioflavour.insa-toulouse.fr).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fani Mantzouridou.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 21 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lalou, S., Mantzouridou, F., Paraskevopoulou, A. et al. Bioflavour production from orange peel hydrolysate using immobilized Saccharomyces cerevisiae . Appl Microbiol Biotechnol 97, 9397–9407 (2013). https://doi.org/10.1007/s00253-013-5181-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-5181-6

Keywords

Navigation