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Phenotypic characterization of indigenous Saccharomyces cerevisiae strains associated with sorghum beer and palm wines

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Abstract

In order to phenotypically characterized Saccharomyces cerevisiae strains isolated from sorghum beer and palm wines for a possible selection of a starter culture, 30 strains were tested for killer activity, temperature resistance, ethanol tolerance, carbohydrate fermentation, enzyme profile and sorghum wort fermentation. Of the tested strains, three showed a killer profile, while four showed a neutral profile and 23 were found to be sensitive to K2 toxin. Temperatures of 40 °C and 44 °C allowed to distinguish strains into four thermal groups with only three strains may grow at 44 °C. Almost tested strains were tolerant to 5% ethanol with viability rates up to 73%. But at 10% and 15% ethanol, respectively 18 and 7 strains were tolerant. Carbohydrate fermentation revealed 13 fermentation profiles, including one typical and 12 atypical profiles. The typical profile strains (16.13% of the strains) fermented glucose, galactose, fructose, sucrose, maltose, trehalose and raffinose. Most of the strains secreted lipases (mainly esterase and esterase-lipase), proteases (mainly valine and cysteine arylamidase, chrymotrypsin) and phosphatases (mainly acid phosphatase and naphthol phosphohydrolase). On contrary, only five strains isolated from sorghum beer exhibited glucosidase activity, mainly α-glucosidase. The analyse of fermented sorghum wort revealed that fermentative performance is strain dependent. Furthermore, the Hierarchical Cluster Analysis showed that the strains were separated in three distinct clusters with the strains from sorghum beer clustered separately.

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References

  • Adewara AO, Ogunbanwo ST (2013) Effects of processing variables on the production of ‘Burukutu’, a Nigerian fermented beverage. Nat Sci 11(1):16–28

    Google Scholar 

  • Ahmed A, Nasim FH, Batool K, Bibi A (2017) Microbial β-glucosidase: sources, production and applications. J Appl Environ Microbiol 1:31–46

    Google Scholar 

  • Aka S, Djeni NT, N’guessan KF, Yao KC, Djè KM (2008) Variabilité des propriétés physico-chimiques et dénombrement de la flore fermentaire du tchapalo, une bière traditionnelle de sorgho en Côte d’Ivoire. Afr Sci 04(2):274–286

    Google Scholar 

  • Aldiguier AS, Alfenore S, Cameleyre X, Goma G, Uribelarrea JL, Guillouet SE, Molina Jouve C (2004) Synergistic temperature and ethanol effect on Saccharomyces cerevisiae dynamic behaviour in ethanol biofuel production. Biop Bios Eng 26:217–222

    CAS  Google Scholar 

  • Amoikon TL, Aké MD, Djéni NT, Grondin C, Casaregola S, Djè KM (2019) Diversity and enzymatic profiles of indigenous yeasts isolated from three types of palm wines produced in Côte d’Ivoire. J Appl Microbiol 126(2):567–579. https://doi.org/10.1111/jam.14154

    Article  CAS  PubMed  Google Scholar 

  • Amoikon TLS, Marcotte S, Djeni NT, N’Sa KMC, Grondin C, Tinsley C, Casaregola S, Dje KM (2020) A study on the potential of yeasts isolated from palm wines to produce flavouring compounds. LWT Food Sci Technol 128:109506. https://doi.org/10.1016/j.lwt.2020.109506

    Article  CAS  Google Scholar 

  • Arroyo-Lopez FN, Orlic S, Querol A, Barrio E (2009) Effects of temperature, pH and sugar concentration on the growth parameters of Saccharomyces cerevisiae, S. kudriavzevii and their interspecific hybrid. Int J Food Microbiol 131:120–127

    Article  CAS  Google Scholar 

  • Ayoub MJ (2006) Diversités moléculaire et phénotypique de souches autochtones œnologiques de Saccharomyces cerevisiae isolées au Liban. Thesis of National Agronomic Institut, Paris-Grignon (INAPG), Paris

    Google Scholar 

  • Banjara N, Nickerson KW, Suhr MJ, Hallen-Adams HE (2016) Killer toxin from several food-derived Debaryomyces hansenii strains effective against pathogenic Candida yeasts. Int J Food Microbiol 222:23–29. https://doi.org/10.1016/j.ijfoodmicro.2016.01.016

    Article  CAS  PubMed  Google Scholar 

  • Bedriñana RP, Simón AQ, Valles BS (2010) Genetic and phenotypic diversity of autochthonous cider yeasts in a cellar from Asturias. Food Microbiol 27:503–508

    Article  Google Scholar 

  • Belda I, Ruiz J, Alonso A, Marquina D, Navascues E, Santos A (2016) Actividades enzimaticas de levaduras no Saccharomyces para su aplicacion enologica. http://www.acenologia.com/cienciaytecnologia/actividades_enzimaticas_no_saccharomyces_cienc0715.htm, pp 1–8

  • Belda I, Ruiz J, Alonso A, Marquina D, Santos A (2017) The biology of Pichia membranifaciens killer toxins. Toxins 9:112. https://doi.org/10.3390/toxins9040112

    Article  CAS  PubMed Central  Google Scholar 

  • Borrull A, Poblet M, Rozès N (2015) New insights into the capacity of commercial wine yeasts to grow on sparkling wine media. Factor screening for improving wine yeast selection. Food Microbiol 48:41–48. https://doi.org/10.1016/j.fm.2014.12.006

    Article  CAS  PubMed  Google Scholar 

  • Camarasa C, Sanchez I, Brial P, Bigey F, Dequin S (2011) Phenotypic landscape of Saccharomyces cerevisiae during wine fermentation: evidence for origin-dependent metabolic traits. PLoS ONE 6:25147. https://doi.org/10.1371/journal.pone.0025147

    Article  CAS  Google Scholar 

  • Coulibaly WH, Cot M, N’guessan KF, Coulibaly I, Rigou P, Djè KM (2018) Ethanol effect on yeast strains isolated from tchapalo, a traditional sorghum beer from Côte d’Ivoire. Int Food Res J 25(2):612–619

    CAS  Google Scholar 

  • Ding J, Huang X, Zhang L, Zhao N, Yang D, Zhang K (2009) Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae. Appl Microbiol Biotechnol 85:253–263. https://doi.org/10.1007/s00253-009-2223-1

    Article  CAS  PubMed  Google Scholar 

  • Djè KM, N’guessan KF, Djeni NT, Dadié AT (2008) Biochemical changes during alcoholic fermentation in the production of tchapalo, a traditional sorghum beer. Int J Food Eng 4(7):1–15. https://doi.org/10.2202/1556-3758.1408

    Article  Google Scholar 

  • Egue A, N’guessan KF, Aka-Gbezo S, Bouatenin KM, Koussemon-Camara M (2018) Candida species in tchapalo and bangui, two traditional alcoholic beverages from Côte d’Ivoire. Fungal Biol 122:283–292

    Article  CAS  Google Scholar 

  • Entian K-D (1997) Sugar phosphorylation in yeast. In: Zimmerman FK, Entian K-D (eds) Yeast sugar metabolism. Technomic Publishing Company, Lancaster, pp 67–79

    Google Scholar 

  • Escribano R, Gonzalez-Arenzana L, Garijo P, Berlanas C, Lopez-Alfaro I, Lopez R, Gutierrez AR, Santamaria P (2017) Screening of enzymatic activities within different enological non-Saccharomyces yeasts. J Food Sci Technol 54(6):1555–1564. https://doi.org/10.1007/s13197-017-2587-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ganga MA, Martinez C (2004) Effect of wine yeast monoculture practice on the biodiversity of non-Saccharomyces yeasts. J Appl Microbiol 96:78–83

    Article  Google Scholar 

  • Greppi A, Rantisou K, Padonou W, Hounhouigan J, Jespersen L, Jakobsen M, Cocolin L (2013) Yeast dynamics during spontaneous fermentation of mawè and tchoukoutou, two traditional products from Benin. Int J Food Microbiol 165:200–207

    Article  CAS  Google Scholar 

  • Ho DH, Powel C (2014) The effect temperature on the growth characteristics of ethanol producing yeast strains. Int J Renew Energy Environ Eng 2(1):1–6

    Google Scholar 

  • Jakobsen M, Narvhus J (1996) Yeasts and their possible beneficial and negative effects on the quality of dairy products. Int Dairy J 6:755–768

    Article  Google Scholar 

  • Jespersen L (2003) Occurrence and taxonomic characteristics of strains of Saccharomyces cerevisiae predominant in African indigenous fermented foods and beverages. FEMS Yeast Res 3(2):191–200

    Article  CAS  Google Scholar 

  • Karamoko D, Djeni NT, N’guessan KF, Bouatenin K, MJ-P, Djè KM (2012) The biochemical and microbiological quality of palm wine samples produced at different periods during tapping and changes which occurred during their storage. Food Control 26(2):504–511

    Article  CAS  Google Scholar 

  • Kreger-van Rij NJW (1984) The yeasts: a taxonomic study. Elsevier, Amsterdam

    Google Scholar 

  • Kubota S, Takeo I, Kume K, Kanai M, Shitamukai A, Mizunuma M, Miyakawa T, Shimoi H, Iefuji H, Hirata D (2004) Effect of ethanol on cell Growth of budding yeast: genes that are important for cell growth in the presence of ethanol. Bios Biotechnol Biochem 68(4):968–972. https://doi.org/10.1271/bbb.68.968

    Article  CAS  Google Scholar 

  • Lopes CA, van Broock M, Querol A, Caballero AC (2002) Saccharomyces cerevisiae wine yeast populations in a cold region in Argentinean Patagonia: a study at different fermentation scales. J Appl Microbiol 93:608–615. https://doi.org/10.1046/j.1365-2672.2002.01738.x

    Article  CAS  PubMed  Google Scholar 

  • Lopes CA, Rodríguez ME, Sangorrín M, Querol A, Caballero AC (2007) Patagonian wines: the selection of an indigenous yeast starter. J Ind Microbiol Biotechnol 34:539–546. https://doi.org/10.1007/s10295-007-0227-3

    Article  CAS  PubMed  Google Scholar 

  • Lu C, Brauer MJ, Botstein D (2009) Slow growth induces heat-shock resistance in normal and respiratory-deficient yeast. Mol Biol Cell 20:891–903. https://doi.org/10.1091/mbc.E08-08-0852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lukaszuk C, Krajewska-Kulak E, Niczyporuk W, Theodosopoulou E, Hatzopulu A, Krawczuk-Rybak M, Wojtukiewicz M (2005) Variations of enzymatic activity and biotypes of the yeast like fungi strains isolated from cancers patients. Adv Appl Math Bios 50:16–19

    CAS  Google Scholar 

  • Morard M, Macías LG, Adam AC, Lairón-Peris M, Pérez-Torrado R, Toft C, Barrio E (2019) Aneuploidy and ethanol tolerance in Saccharomyces cerevisiae. Front Gen 10:82. https://doi.org/10.3389/fgene.2019.00082

    Article  CAS  Google Scholar 

  • N’guessan FK, N’Dri DY, Camara F, Djè KM (2010) Saccharomyces cerevisiae and Candida tropicalis as starter cultures for the alcoholic fermentation of tchapalo, a traditional sorghum beer. World J Microbiol Biotechnol 26:693–699. https://doi.org/10.1007/s11274-009-0224-y

    Article  CAS  Google Scholar 

  • N’guessan KF, Brou K, Noémie J, Casaregola S, Djè KM (2011) Identification of yeasts during alcoholic fermentation of tchapalo, a traditional sorghum beer from Côte d’Ivoire. Antonie Van Leeuwenhoek 99(4):855–864

    Article  Google Scholar 

  • Pramateftaki PV, Lanaridis P, Typas MA (2000) Molecular identification of wine yeasts at species or strain level: a case study with strains from two vine-growing areas of Greece. J Appl Microbiol 89(2):236–248

    Article  CAS  Google Scholar 

  • Reifenberger E, Freidel K, Ciriacy M (1995) Identification of novel HXT genes in Saccharomyces cerevisiae reveals the impact of individual hexose transporters on glycolytic flux. Mol Microbiol 16:157–167

    Article  CAS  Google Scholar 

  • Renault P (2010) Caractérisation phénotypique de l’espèce Torulaspora delbrueckii en conditions œnologiques. Applications à la co-inoculation avec l’espèce Saccharomyces cerevisiae. Thesis of University Bordeaux 2, Bordeaux

    Google Scholar 

  • Romano P, Capece A, Serafino V, Romaniello R, Poeta C (2008) Biodiversity of wild strains of Saccharomyces cerevisiae as tool to complement and optimize wine quality. World J Microbiol Biotechnol 24:1797–1802. https://doi.org/10.1007/s11274-008-9672-z

    Article  CAS  Google Scholar 

  • Santamarıa P, Lopez R, Portu J, Gonzalez-Arenzana L, Lopez-Alfaro I, Gutierrez AR, Garde-Cerdan T (2015) Role of phenylalanine in Viticulture and Enology. In: Elliamson D (ed) Phenylalanine. Dietary, sources, functions and health effects. Nova Publisher, New York, pp 49–70

    Google Scholar 

  • Schuller D, Alves H, Dequin S, Casal M (2005) Ecological survey of Saccharomyces cerevisiae strains from vineyards in the Vinho Verde region of Portugal. FEMS Microbiol Ecol 51:167–177

    Article  CAS  Google Scholar 

  • Tofalo R, Perpetuini G, Fasoli G, Schirone M, Corsetti A, Suzzi G (2014) Biodiversity study of wine yeasts belonging to the “terroir” of Montepulciano d’Abruzzo “Colline Teramane” revealed Saccharomyces cerevisiae strains exhibiting a typical and “unique 5.8S-ITS restriction patterns.” Food Microbiol 39:7–12. https://doi.org/10.1016/j.fm.2013.10.001

    Article  CAS  PubMed  Google Scholar 

  • Tra Bi YC, Amoikon LST, Kouakou AC, Noemie J, Lucas M, Grondin C, Legras J-L, N’guessan KF, Djeni NT, Djè KM, Casaregola S (2019) Genetic diversity and population structure of Saccharomyces cerevisiae strains isolated from traditional alcoholic beverages of Côte d’Ivoire. Int J Food Microbiol 297:1–10

    Article  CAS  Google Scholar 

  • Van der Aa Kühle A, Jesperen L, Glover RLK, Diawara B, Jakobsen M (2001) Identification and characterization of Saccharomyces cerevisiae strains isolated from West African sorghum beer. Yeast 18:1069–1079

    Article  Google Scholar 

  • Versavaud A, Courcoux P, Roulland C, Dulau L, Hallet J-N (1995) Genetic diversity and geographical distribution of wild Saccharomyces cerevisiae strains from the wine-producing area of Charentes, France. Appl Environ Microbiol 61(10):3521–3529

    Article  CAS  Google Scholar 

  • Wang X, Li S, Yang X, Yang S, Zhu M (2012) Technology prospecting on enzymes: application. Market Eng 2(3):1–11

    Google Scholar 

  • Zagorc T, Mar·z A, Cadez N, Povhe Jemec K, Pèter G, Resnik M, Nemanië J, Raspor P (2001) Indigenous wine killer yeasts and their application as starter culture in wine fermentation. Food Microbiol 18:441–451

    Article  CAS  Google Scholar 

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Acknowledgements

This work was financially supported by the International Foundation for Science, Sweden (Grant No. E/5560-1) and the National Institute for Agricultural Research (INRA, France). We tank Dr. Christelle Louis-Mondésir for expert technical assistance.

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Authors and Affiliations

  1. Institut de Recherche sur les Energies Nouvelles (IREN), Université Nangui Abrogoua, 02 BP 801, Abidjan 02, Côte d’Ivoire

    Charles Y. Tra Bi

  2. Laboratoire de Biotechnologie et Microbiologie des Aliments, Unité de Formation et de Recherche en Sciences et Technologie des Aliments (UFR-STA), Université Nangui Abrogoua, 02 BP 801, Abidjan 02, Côte d’Ivoire

    Clémentine A. Kouakou-Kouamé, Florent K. N’guessan & Marcellin K. Djè

  3. Centre de Coopération Internationale en Recherche Agronomique pour le Développement, CIRAD, UMR Qualisud, TA 95B/16, 34398, Montpellier Cedex 5, France

    Didier Montet

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  1. Charles Y. Tra Bi
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  2. Clémentine A. Kouakou-Kouamé
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  3. Florent K. N’guessan
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Correspondence to Florent K. N’guessan.

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Tra Bi, C.Y., Kouakou-Kouamé, C.A., N’guessan, F.K. et al. Phenotypic characterization of indigenous Saccharomyces cerevisiae strains associated with sorghum beer and palm wines. World J Microbiol Biotechnol 37, 24 (2021). https://doi.org/10.1007/s11274-020-02990-4

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