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Yeast species diversity in apple juice for cider production evidenced by culture-based method

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Abstract

Identification of yeasts isolated from apple juices of two cider houses (one located in a plain area and one in an alpine area) was carried out by culture-based method. Wallerstein Laboratory Nutrient Agar was used as medium for isolation and preliminary yeasts identification. A total of 20 species of yeasts belonging to ten different genera were identified using both BLAST algorithm for pairwise sequence comparison and phylogenetic approaches. A wide variety of non-Saccharomyces species was found. Interestingly, Candida railenensis, Candida cylindracea, Hanseniaspora meyeri, Hanseniaspora pseudoguilliermondii, and Metschnikowia sinensis were recovered for the first time in the yeast community of an apple environment. Phylogenetic analysis revealed a better resolution in identifying Metschnikowia and Moesziomyces isolates than comparative analysis using the GenBank or YeastIP gene databases. This study provides important data on yeast microbiota of apple juice and evidenced differences between two geographical cider production areas in terms of species composition.

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References

  • Baffi MA, Tobal T, Ghilardi Lago JE, Boscolo M, Gomes E, Da-Silva R (2013) Wine aroma improvement using a β-glucosidase preparation from Aureobasidium pullulans. Appl Biochem Biotechnol 169:493–501

    Article  CAS  Google Scholar 

  • Brežná B, Ženišová K, Chovanová K, Chebeňová V, Kraková L, Kuchta T, Pangallo D (2010) Evaluation of fungal and yeast diversity in Slovakian wine-related microbial communities. Antonie Leeuwenhoek 98:519–552

    Article  Google Scholar 

  • Cabranes C, Moreno J, Mangas JJ (1990) Dynamics of yeast populations during cider fermentation in the asturian region of Spain. Appl Environ Microbiol 56:3881–3884

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cadete RM, Cheab MAM, Santos RO, Safar SVB, Zilli JE, Vital MJS, Basso LC, Lee C-F, Kurtzman CP, Lachance M-A, Rosa CA (2015) Cyberlindnera xylosilytica sp. nov., a xylitol-producing yeast species isolated from lignocellulosic materials. Int J Syst Evol Microbiol 65:2968–2974

    Article  CAS  Google Scholar 

  • Cadez N, Raspor P, Smith MT (2006) Phylogenetic placement of Hanseniaspora–Kloeckera species using multigene sequence analysis with taxonomic implications: descriptions of Hanseniaspora pseudoguilliermondii sp. nov. and Hanseniaspora occidentalis var. citrica var. nov. Int J Syst Evol Microbiol 56:1157–1165

    Article  CAS  Google Scholar 

  • Capozzi V, Garofalo C, Chiriatti MA, Grieco F, Spano G (2015) Microbial terroir and food innovation: the case of yeast biodiversity in wine. Microbiol Res 181:75–83

    Article  CAS  Google Scholar 

  • Chen W, Qi-Ming W, Jian-Hua JIA, Feng-Yan BAI (2009) Candida pseudocylindracea sp. nov. and Candida wuzhishanensis sp. nov. from Hainan Island, southern China. Mycosystema 28:79–85

    CAS  Google Scholar 

  • Chovanová K, Kraková L, Ženišová K, Turcovská V, Brežná B, Kuchta T, Pangallo D (2011) Selection and identification of autochthonous yeasts in Slovakian wine samples using a rapid and reliable three-step approach. Lett Appl Microbiol 53:231–237

    Article  Google Scholar 

  • Cocolin L, Bisson LF, Mills DA (2000) Direct profiling of the yeast dynamics in wine fermentations. FEMS Microbiol Lett 189:81–87

    Article  CAS  Google Scholar 

  • Coton E, Coton M, Levert D, Casaregola S, Sohier D (2006) Yeast ecology in French cider and black olive natural fermentations. Int J Food Microbiol 108:130–135

    Article  CAS  Google Scholar 

  • Cousin FJ, Le Guellec R, Schlusselhuber M, Dalmasso M, Laplace J-M, Cretenet M (2017) Microorganisms in fermented apple beverages: current knowledge and future directions. Microorganisms 39:1–22

    Google Scholar 

  • Daniel H-M, Lachance M-A, Kurtzman CP (2014) On the reclassification of species assigned to Candida and other anamorphic ascomycetous yeast genera based on phylogenetic circumscription. Antonie Leeuwenhoek 106:67–84

    Article  Google Scholar 

  • de Vega C, Guzmán B, Steenhuisen S-L, Johnson SD, Herrera CM, Lachance M-A (2014) Metschnikowia drakensbergensis sp. nov. and Metschnikowia caudata sp. nov., endemic yeasts associated with Protea flowers in South Africa. Int J Syst Evol Microbiol 64:3724–3732

    Article  Google Scholar 

  • Glushakova AM, Kachalkin AV (2017) Endophytic yeasts in Malus domestica and Pyrus communis fruits under anthropogenic impact. Microbiology 86:128–135

    Article  CAS  Google Scholar 

  • Graça A, Santo D, Esteves E, Nunes C, Abadias M, Quintas C (2015) Evaluation of microbial quality and yeast diversity in fresh-cut apple. Food Microbiol 51:179–185

    Article  Google Scholar 

  • Haider W, Barillier D, Hayat A, Gaillarda JL, Ledauphina J (2014) Rapid quantification and comparison of major volatile compounds of ciders from France (Normandy and Brittany) using microextraction by packed sorbent (MEPS). Anal Methods 6:1364–1376

    Article  CAS  Google Scholar 

  • Johnson E (2013) Biotechnology of non-Saccharomyces yeast—the basidiomycestes. Appl Microbiol Biotechnol 97:7563–7577

    Article  CAS  Google Scholar 

  • Joshi VK, Attri BL (2017) Specific features of table wine production technologies. In: Kosseva MR, Joshi VK, Panesar PS (eds) Science and technology of fruit wine production. Elsevier, Amsterdam

    Google Scholar 

  • Kachalkin AV, Abdullabekova DA, Magomedova ES, Magomedov GG, Chernov IY (2015) Yeasts of the vineyards in Dagestan and other regions. Microbiology 84:425–432

    Article  CAS  Google Scholar 

  • Kruse J, Doehlemann G, Kemen E, Thines M (2017) Asexual and sexual morphs of Moesziomyces revisited. IMA Fungus 8:117–129

    Article  Google Scholar 

  • Kurtzman CP (2000) Four new yeasts in the Pichia anomala clade. Int J Syst Evol Microbiol 50:395–404

    Article  Google Scholar 

  • Kurtzman CP (2005) New species and a new combination in the Hyphopichia and Yarrowia yeast clades. Antonie Leeuwenhoek 88:121–130

    Article  CAS  Google Scholar 

  • Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Leeuwenhoek 73:331–371

    Article  CAS  Google Scholar 

  • Kurtzman CP, Suzuki M (2010) Phylogenetic analysis of ascomycete yeasts that form coenzyme Q-9 and the proposal of the new genera Babjeviella, Meyerozyma, Millerozyma, Priceomyces, and Scheffersomyces. Mycoscience 51:2–14

    Article  CAS  Google Scholar 

  • Kurtzman CP, Robnett CJ, Yarrow D (2001) Three new species of Candida from apple cider: C. anglica, C. cidri, and C. pomicola. Antonie Leeuwenhoek 80:237–244

    Article  CAS  Google Scholar 

  • Kurtzman CP, Mateo RQ, Kolecka A, Theelen B, Robert V, Boekhout T (2015) Advances in yeast systematics and phylogeny and their use as predictors of biotechnologically important metabolic pathways. FEMS Yeast Res, 1–15

  • Limtong S, Nitiyon S, Kaewwichian R, Jindamorakot S, Am-In S, Yongmanitchai W (2012) Wickerhamomyces xylosica sp. nov. and Candida phayaonensis sp. nov., two xylose-assimilating yeast species from soil. Int J Syst Evol Microbiol 62:2786–2792

    Article  CAS  Google Scholar 

  • Morrissey WF, Davenport B, Querol A, Dobson ADW (2004) The role of indigenous yeasts in traditional Irish cider fermentations. J Appl Microbiol 97:647–655

    Article  CAS  Google Scholar 

  • Naseeb S, James SA, Alsammar H, Michaels CJ, Gini BG, Nueno-Palop C, Bond CJ, McGhie E, Roberts JN, Delneri D (2017) Saccharomyces jurei sp. nov., isolation and genetic identification of a novel yeast species from Quercus robur. Int J Syst Evol Microbiol 67:2046–2052

    Article  Google Scholar 

  • Ouoba LII, Nielsen DS, Anyogu A, Kando C, Diawara B, Jespersen L, Sutherland JP (2015) Hanseniaspora jakobsenii sp. nov., a yeast isolated from Bandji, a traditional palm wine of Borassus akeassii. Int J Syst Evol Microbiol 65:3576–3579

    Article  Google Scholar 

  • Pallmann CL, Brown JA, Olineka TL, Cocolin L, Mills DA, Bisson LF (2001) Use of WL medium to profile native flora fermentations. Am J Enol Vitic 52:198–203

    CAS  Google Scholar 

  • Pando Bedriñana P, Querol Simón A, Suárez Valles B (2010) Genetic and phenotypic diversity of autochthonous cider yeasts in a cellar from Asturias. Food Microbiol 27:503–508

    Article  Google Scholar 

  • Passoth V (2016) Yeast previously included in the genus Pichia. In: Paterson RRM, Lima N (eds) Molecular biology of food and water borne mycotoxigenic and mycotic fungi. Taylor and Francis Group, Boca Raton, pp 463–482

    Google Scholar 

  • Pelliccia C, Antonielli L, Corte L, Bagnetti A, Fatichenti F, Cardinali G (2011) Preliminary prospection of the yeast biodiversity on apple and pear surfaces from Northern Italy orchards. Ann Microbiol 61:965–972

    Article  CAS  Google Scholar 

  • Picinelli Lobo A, Antón-Díaz MS, Mangas Alonso JJ, Suárez Valles B (2016) Characterization of Spanish ciders by means of chemical and olfactometric profiles and chemometrics. Food Chem 213:505–513

    Article  CAS  Google Scholar 

  • Polizzotto G, Barone E, Ponticello G, Fasciana T, Barbera D, Corona O, Amore G, Giammanco A, Oliva D (2016) Isolation, identification and oenological characterization of non-Saccharomyces yeasts in a Mediterranean island. Lett Appl Microbiol 63:131–138

    Article  CAS  Google Scholar 

  • Suárez Valles B, Pando Bedriñana R, Fernández Tascón N, Querol Simón A, Rodríguez Madrera R (2007) Yeast species associated with the spontaneous fermentation of cider. Food Microbiol 24:25–31

    Article  Google Scholar 

  • Varela C (2016) The impact of non-Saccharomyces yeast in the production of alcoholic beverages. Appl Microbiol Biotechnol 100:9861–9874

    Article  CAS  Google Scholar 

  • Wang H, Hu Z, Long F, Niu C, Yuan Y, Yue T (2015) Characterization of osmotolerant yeasts and yeast-like molds from apple orchards and apple juice processing plants in China and investigation of their spoilage potential. J Food Sci 80:1850–1860

    Article  Google Scholar 

  • Wei J, Niu C, Liu B, Yuan Y, Yue T (2017) Identification and characterization of epiphytic yeasts on apples in China. RSC Adv 7:44766–44772

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Zalar P, Gostinčar C, de Hoog GS, Uršič V, Sudhadham M, Gunde-Cimerman N (2008) Redefinition of Aureobasidium pullulans and its varieties. Stud Mycol 61:21–38

    Article  CAS  Google Scholar 

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Correspondence to Marilinda Lorenzini.

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Lorenzini, M., Simonato, B. & Zapparoli, G. Yeast species diversity in apple juice for cider production evidenced by culture-based method. Folia Microbiol 63, 677–684 (2018). https://doi.org/10.1007/s12223-018-0609-0

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  • DOI: https://doi.org/10.1007/s12223-018-0609-0