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Immobilized enzymes from Geotrichum spp. improve wine quality

  • Biotechnologically relevant enzymes and proteins
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Abstract

Higher alcohols are the byproducts of yeasts in alcohol fermentation and are harmful to human health at high concentrations. In this study, immobilized crude enzymes extracted from Geotrichum spp. strains S12 and S13 were separately employed to treat red wine, then GC and GC-MS analyses were used to determine the profiles of volatile compounds in untreated and treated wine samples. Immobilized enzymes from S13 (SA-S13E) were more active in decreasing higher alcohols than enzymes from S12. Conditions for preparing SA-S13E were optimized, and best results were obtained at a sodium alginate concentration of 35 g/L, calcium chloride of 20 g/L, and crude enzyme dosage of 3 mL. Treatment with SA-S13E significantly increased the ester content and sensory quality of wine. After being reused three times, SA-S13E still exhibited approximately 80% activity towards 1-propanol, isobutanol, and hexanol and had certain activity even after 3 months storage at −20 °C, indicating high stability in application and storage and thus showing potential in wine processing.

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References

  • Agouridis N, Kopsahelis N, Plessas S, Koutinas AA, Kanellaki M (2008) Oenococcus oeni cells immobilized on delignified cellulosic material for malolactic fermentation of wine. Bioresour Technol 99:9017–9020. doi:10.1016/j.biortech.2008.04.026

    Article  CAS  PubMed  Google Scholar 

  • Ancín C, Ayestarán B, Corroza M, Garrido J, González A (1996) Influence of prefermentation clarification on the higher alcohol contents of wines. Food Chem 55:241–249. doi:10.1016/0308-8146(95)00125-5

    Article  Google Scholar 

  • Aranaz I, Acosta N, Férnandez-Valle ME, Heras A (2015) Optimization of D-amino acid production catalyzed by immobilized multi-enzyme system in polyelectrolyte complex gel capsules. J Mol Catal B-Enzym 121:45–52. doi:10.1016/j.molcatb.2015.06.003

    Article  CAS  Google Scholar 

  • Armada L, Fernández E, Falqué E (2010) Influence of several enzymatic treatments on aromatic composition of white wines. LWT - Food Sci Technol 43:1517–1525. doi:10.1016/j.lwt.2010.06.009

    Article  CAS  Google Scholar 

  • Atacan K, Cakiroglu B, Ozacar M (2016) Improvement of the stability and activity of immobilized trypsin on modified Fe3O4 magnetic nanoparticles for hydrolysis of bovine serum albumin and its application in the bovine milk. Food Chem 212:460–468. doi:10.1016/j.foodchem.2016.06.011

    Article  CAS  PubMed  Google Scholar 

  • Bindon K, Varela C, Kennedy J, Holt H, Herderich M (2013) Relationships between harvest time and wine composition in Vitis vinifera L. cv. Cabernet Sauvignon 1. Grape and wine chemistry. Food Chem 138:1696–1705. doi:10.1016/j.foodchem.2012.09.146

    Article  CAS  PubMed  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. doi:10.1111/j.1567-1364.2008.00412.x

    Article  CAS  PubMed  Google Scholar 

  • Chan ES, Lee BB, Ravindra P, Poncelet D (2009) Prediction models for shape and size of ca-alginate macrobeads produced through extrusion-dripping method. J Colloid Interf Sci 338:63–72. doi:10.1016/j.jcis.2009.05.027

    Article  CAS  Google Scholar 

  • Chang AC (2003) The effects of gamma irradiation on rice wine maturation. Food Chem 83:323–327. doi:10.1016/S0308-8146(03)00050-5

    Article  CAS  Google Scholar 

  • Estévez P, Gil ML, Falqué E (2004) Effects of seven yeast strains on the volatile composition of Palomino wines. Int J Food Sci Tech 39:61–69. doi:10.1046/j.0950-5423.2003.00755.x

    Article  Google Scholar 

  • Fan W, Qian MC (2006) Identification of aroma compounds in Chinese ‘Yanghe Daqu’ liquor by normal phase chromatography fractionation followed by gas chromatography [sol] olfactometry. Flavour Frag J 21:333–342. doi:10.1002/ffj.1621

    Article  CAS  Google Scholar 

  • Gueguen Y, Chemardin P, Janbon G, Arnaud A, Galzy P (1996) A very efficient β-glucosidase catalyst for the hydrolysis of flavor precusors of wines and fruit juices. J Agr Food Chem 44:2336–2340. doi:10.1021/jf950360j

    Article  CAS  Google Scholar 

  • Han QA, Shi JL, Zhu J, Lv HL, Du SK (2014) Enzymes extracted from apple peels have activity in reducing higher alcohols in Chinese liquors. J Agr Food Chem 62:9529–9538. doi:10.1021/jf5018862

    Article  CAS  Google Scholar 

  • Hazelwood LA, Daran JM, van Maris AJA, Pronk JT, Dickinson JR (2008) The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl Environ Microbiol 74:2259–2266. doi:10.1128/AEM.02625-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hevia K, Castro R, Natera R, González-García JA, Barroso CG, Durán-Guerrero E (2016) Optimization of head space sorptive extraction to determine volatile compounds from oak wood in fortified wines. Chromatographia 79:763–771. doi:10.1007/s10337-016-3088-y

    Article  CAS  Google Scholar 

  • Klosowski G, Mikulski D, Czuprynski B, Kotarska K (2010) Characterisation of fermentation of high-gravity maize mashes with the application of pullulanase, proteolytic enzymes and enzymes degrading non-starch polysaccharides. J Biosci Bioeng 109:466–471. doi:10.1016/j.jbiosc.2009.10.024

    Article  CAS  PubMed  Google Scholar 

  • Kodama Y, Omura F, Miyajima K, Ashikari T (2001) Control of higher alcohol production by manipulation of the BAP2 gene in brewing yeast. J Am Soc Brew Chem 59:157–162

    CAS  Google Scholar 

  • Komes D, Ulrich D, Ganic KK, Lovric T (2007) Study of phenolic and volatile composition of white wine during fermentation and a short time of storage. Vitis 46:77–84

    Google Scholar 

  • Kourkoutas Y, Bekatorou A, Banat IM, Marchant R, Koutinas AA (2004) Immobilization technologies and support materials suitable in alcohol beverages production: a review. Food Microbiol 21:377–397. doi:10.1016/j.fm.2003.10.005

    Article  CAS  Google Scholar 

  • Lee BB, Ravindra P, Chan ES (2013) Size and shape of calcium alginate beads produced by extrusion dripping. Chem Eng Technol 36:1627–1642. doi:10.1002/ceat.201300230

    CAS  Google Scholar 

  • Lessard MH, Viel C, Boyle B, St-Gelais D, Labrie S (2014) Metatranscriptome analysis of fungal strains Penicillium camemberti and Geotrichum candidum reveal cheese matrix breakdown and potential development of sensory properties of ripened Camembert-type cheese. BMC Genomics 15:235. doi:10.1186/1471-2164-15-235

    Article  PubMed  PubMed Central  Google Scholar 

  • Mallouchos A, Konaitis M, Koutinas A, Kanellaki M (2003) Wine fermentations by immobilized and free cells at different temperatures. Effect of immobilization and temperature on volatile by-products. Food Chem 80:109–113. doi:10.1016/S0308-8146 (02)00247-9

    Article  CAS  Google Scholar 

  • Mateo C, Palomo JM, Fernandez-Lorente G, Guisan JM, Fernandez-Lafuente R (2007) Improvement of enzyme activity, stability and selectivity via immobilization techniques. Enzym Microb Technol 40:1451–1463. doi:10.1016/j.enzmictec.2007.01.018

    Article  CAS  Google Scholar 

  • Mdaini N, Gargouri M, Hammami M, Monser L, Hamdi M (2006) Production of natural fruity aroma by Geotrichum candidum. Appl Biochem Biotech 128:227–235. doi:10.1385/ABAB:128:3:227

    Article  CAS  Google Scholar 

  • Molina AM, Swiegers JH, Varela C, Pretorius IS, Agosin E (2007) Influence of wine fermentation temperature on the synthesis of yeast-derived volatile aroma compounds. Appl Microbiol Biotechnol 77:675–687. doi:10.1007/s00253-007-1194-3

    Article  CAS  PubMed  Google Scholar 

  • Procopio S, Qian F, Becker T (2011) Function and regulation of yeast genes involved in higher alcohol and ester metabolism during beverage fermentation. Eur Food Res Technol 233:721–729. doi:10.1007/s00217-011-1567-9

    Article  CAS  Google Scholar 

  • Rodriguez-Bencomo JJ, Munoz-Gonzalez C, Andujar-Ortiz I, Martin-Alvarez PJ, Moreno-Arribas MV, Pozo-Bayon MA (2011) Assessment of the effect of the non-volatile wine matrix on the volatility of typical wine aroma compounds by headspace solid phase microextraction/gas chromatography analysis. J Sci Food Agr 91:2484–2494. doi:10.1002/jsfa.4494

    Article  CAS  Google Scholar 

  • Rous CV, Snow R, Kunkee RE (1983) Reduction of higher alcohols by fermentation with a leucine-auxotrophic mutant of wine yeast. J Inst Brew 89:274–278. doi:10.1002/j.2050-0416.1983.tb04185.x

    Article  CAS  Google Scholar 

  • Schoffelen S, van Hest JCM (2012) Multi-enzyme systems: bringing enzymes together in vitro. Soft Matter 8:1736–1746. doi:10.1039/C1SM06452E

    Article  CAS  Google Scholar 

  • Servili M, Begliomini AL, Montedoro G, Petruccioli M, Federici F (1992) Utilisation of a yeast pectinase in olive oil extraction and red wine making processes. J Sci Food Agr 58:253–260. doi:10.1002/jsfa.2740580214

    Article  CAS  Google Scholar 

  • Shen N, Wang JJ, Liu CF, Li YX, Li Q (2014) Domesticating brewing yeast for decreasing acetaldehyde production and improving beer flavor stability. Eur Food Res Technol 238:347–355. doi:10.1007/s00217-014-2169-0

    Article  CAS  Google Scholar 

  • Shi SB, Si T, Liu ZH, Zhang HF, Ang EL, Zhao HM (2016) Metabolic engineering of a synergistic pathway for n-butanol production in Saccharomyces cerevisiae. Sci Rep-UK 6:25675. doi:10.1038/srep25675

    Article  CAS  Google Scholar 

  • Shrinivas D, Kumar R, Naik GR (2012) Enhanced production of alkaline thermostable keratinolytic protease from calcium alginate immobilized cells of thermoalkalophilic Bacillus halodurans JB 99 exhibiting dehairing activity. J Ind Microbiol Biotechnol 39:93–98. doi:10.1007/s10295-011-1003-y

    Article  CAS  PubMed  Google Scholar 

  • Song JQ, Li H, Liang YY, Tao YS, Mi CQ, Qian MC, Wang H (2013) Characterisation of volatile components of red and sparkling wines from a new wine grape cultivar 'Meili' (Vitis vinifera L.) Vitis 52:41–48

    CAS  Google Scholar 

  • Stribny J, Gamero A, Pérez-Torrado R, Querol A (2015) Saccharomyces kudriavzevii and Saccharomyces uvarum differ from Saccharomyces cerevisiae during the production of aroma-active higher alcohols and acetate esters using their amino acidic precursors. Int J Food Microbiol 205:41–46. doi:10.1016/j.ijfoodmicro.2015.04.003

    Article  CAS  PubMed  Google Scholar 

  • Vidal EE, de Billerbeck GM, Simoes DA, Schuler A, Francois JM, de Morais MA (2013) Influence of nitrogen supply on the production of higher alcohols/esters and expression of flavour-related genes in cachaca fermentation. Food Chem 138:701–708. doi:10.1016/j.foodchem.2012.10.147

    Article  CAS  PubMed  Google Scholar 

  • Vilanova M, Siebert TE, Varela C, Pretorius IS, Henschke PA (2012) Effect of ammonium nitrogen supplementation of grape juice on wine volatiles and non-volatiles composition of the aromatic grape variety Albariño. Food Chem 133:124–131. doi:10.1016/j.foodchem.2011.12.082

    Article  CAS  Google Scholar 

  • Xu R, Si YF, Wu XT, Li FT, Zhang BR (2014) Triclosan removal by laccase immobilized on mesoporous nanofibers: strong adsorption and efficient degradation. Chem Eng J 255:63–70. doi:10.1016/j.cej.2014.06.060

    Article  CAS  Google Scholar 

  • Zhang CY, Qi YN, Ma HX, Li W, Dai LH, Xiao DG (2015) Decreased production of higher alcohols by Saccharomyces cerevisiae for Chinese rice wine fermentation by deletion of bat aminotransferases. J Ind Microbiol Biot 42:617–625. doi:10.1007/s10295-015-1583-z

    Article  CAS  Google Scholar 

  • Zhang J, Shi J, Lv H, Liu Y (2013) Induction of hexanol dehydrogenase in Geotrichum spp. by the addition of hexanol. Appl Microbiol Biotechnol 97:1279–1287. doi:10.1007/s00253-012-4280-0

    Article  CAS  PubMed  Google Scholar 

  • Zhen D, Lv M, Chen MB, Luo JJ, Liu DQ (2014) Effects of a mutated yeast plus addition of sucrose and nitrogen on the total higher alcohol levels of a plum wine fermentation. J Inst Brew 120:571–574. doi:10.1002/jib.163

    CAS  Google Scholar 

  • Zhu J, Lu K, Xu X, Wang X, Shi J (2017) Purification and characterization of a novel glutamate dehydrogenase from Geotrichum candidum with higher alcohol and amino acid activity. AMB Express 7:9. doi:10.1186/s13568-016-0307-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Shi JL, Lu Y, Liu LP, Liu YL (2016) Application of strains of Geotrichum spp. to decrease higher alcohols and to increase esters. J Inst Brew 122:147–155. doi:10.1002/jib.287

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the National Key Technology R&D Program (No. 2015BAD16B02); the Agriculture Department of China (Grant No. CARS-30); the Fundamental Research Funds for the Central Universities (3102016QD089); the Fundamental Research Funds for the Central Universities (3102016QD075); the Provincial Scientific Project of Henan (Grant No. 152102210221); and the Scientific Project of Xinyang (Grant No. 150018).

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Authors and Affiliations

  1. Key Laboratory for Space Bioscience and Biotechnology, School of Life Sciences, Northwestern Polytechnical University, 127 Youyi West Road, Xi’an, Shaanxi Province, 710072, China

    Yao Lu, Jing Zhu, Junling Shi, Dongyan Shao & Chunmei Jiang

  2. Department of Food Science, Xinyang College of Agriculture and Forestry, New 24 Street of Yangshan New District, Xinyang, Henan Province, 464000, China

    Jing Zhu

  3. College of Enology, Northwest A&F University, 22 Xinong Road, Yangling, Shaanxi Province, 712100, China

    Yanlin Liu

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  1. Yao Lu
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  2. Jing Zhu
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  3. Junling Shi
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  4. Yanlin Liu
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  6. Chunmei Jiang
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Correspondence to Junling Shi.

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Lu, Y., Zhu, J., Shi, J. et al. Immobilized enzymes from Geotrichum spp. improve wine quality. Appl Microbiol Biotechnol 101, 6637–6649 (2017). https://doi.org/10.1007/s00253-017-8424-0

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  • DOI: https://doi.org/10.1007/s00253-017-8424-0

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