Annals of Microbiology

, Volume 67, Issue 1, pp 99–109 | Cite as

Characterisation of yeast microbiota, chemical and sensory properties of organic and biodynamic Sangiovese red wines

  • Francesca Patrignani
  • Chiara Montanari
  • Diana I. Serrazanetti
  • Giacomo Braschi
  • Pamela Vernocchi
  • Giulia Tabanelli
  • Giuseppina P. Parpinello
  • Andrea Versari
  • Fausto Gardini
  • Rosalba LanciottiEmail author
Original Article


Wine quality is closely linked to the fermentation step, which is driven by the microbial ecology of grape and the use of selected microbial strains as well. The microbial species developing during fermentation determines the type and concentration of many substances, which contribute to the sensory properties of wine and its safety. In this view, the present work aims to characterise the yeast microbiota, chemical and sensory properties of Sangiovese red wines obtained from both biodynamic and organic agriculture. The natural yeast populations of grape musts and their evolution during spontaneous were monitored and investigated. In addition, the volatile composition, physico-chemical and safety features (ethyl-carbamate) and sensory properties of wines were evaluated. The results showed that the yeast population was mostly related to the grape management, i.e. organic or biodynamic, while the wine composition was mainly affected by the winemaking process, and then by the grape management.


Biogenic amines Grape microbial population Spontaneous fermentation Sustainable winemaking 


  1. Albertin W, Miot-Sertier C, Bely M, Marullo P, Coulon J, Moine V, Colonna-Ceccaldi B, Masneuf-Pomarede I (2014) Oenological prefermentation practices strongly impact yeast population dynamics and alcoholic fermentation kinetics in Chardonnay grape must. Int J Food Microbiol 178:87–97. doi: 10.1016/j.ijfoodmicro.2014.03.009 CrossRefPubMedGoogle Scholar
  2. Barata A, Malfeito-Ferreira M, Loureiro V (2012) Changes in sour rotten grape berry microbiota during ripening and wine fermentation. Int J Food Microbiol 154:152–161. doi: 10.1016/j.ijfoodmicro.2011.12.029 CrossRefPubMedGoogle Scholar
  3. Berg J, Tom-Petersen A, Nybroe O (2005) Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Lett Appl Microbiol 40:146–151CrossRefPubMedGoogle Scholar
  4. Capece A, Pietrafesa R, Romano P (2011) Experimental approach for target selection of wild wine yeasts from spontaneous fermentation of “Inzolia” grapes. World J Microbiol Biotechnol 27:2775–2783. doi: 10.1007/s11274-011-0753-z CrossRefGoogle Scholar
  5. 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. doi: 10.1016/j.micres.2015.10.005 CrossRefPubMedGoogle Scholar
  6. Ciani M, Beco L, Comitini F (2006) Fermentation behaviour and metabolic interactions of multistarter wine yeast fermentations. Int J Food Microbiol 108:239–245CrossRefPubMedGoogle Scholar
  7. Comitini F, Gobbi M, Domizio P, Romani C, Lencioni L, Mannazzu I, Ciani M (2011) Selected non-Saccharomyces wine yeasts in controlled multistarter fermentations with Saccharomyces cerevisiae. Food Microbiol 28:873–882. doi: 10.1016/ CrossRefPubMedGoogle Scholar
  8. Domizio P, Liu Y, Bisson LF, Barile D (2014) Use of non-Saccharomyces wine yeasts as novel sources of mannoproteins in wine. Food Microbiol 43:5–15. doi: 10.1016/ CrossRefPubMedGoogle Scholar
  9. Drumonde-Neves J, Franco-Duarte R, Lima T, Schuller D, Pais C (2016) Yeast Biodiversity in Vineyard Environments Is Increased by Human Intervention. PLOSONE| 11:1--13Google Scholar
  10. Englezos V, Rantsiou K, Cravero F, Torchio F, Ortiz-Julien A, Gerbi V, Rolle L, Cocolin L (2016) Starmerella bacillaris and Saccharomyces cerevisiae mixed fermentations to reduce ethanol content in wine. Appl Microbiol Biotechnol 100:5515–5526. doi: 10.1007/s00253-016-7413-z CrossRefPubMedGoogle Scholar
  11. European Union (1990) Commission Regulation (EEC) No. 2676/90 of 17 September 1990 determining Community methods for the analysis of wines. Off J Eur Communities 272:64–73Google Scholar
  12. Francesca N, Chiurazzi M, Romano R, Aponte M, Settanni L, Moschetti G (2010) Indigenous yeast communities in the environment of “Rovello bianco” grape variety and their use in commercial White wine fermentation. World J Microbiol Biotechnol 26:337–351. doi: 10.1007/s11274-009-0181-5 CrossRefGoogle Scholar
  13. Francesca N, Canale DE, Settanni L, Moschetti G (2012) Dissemination of wine-related yeasts by migratory birds. Environ Microbiol Rep 4:105–112. doi: 10.1111/j.1758-2229.2011.00310.x CrossRefPubMedGoogle Scholar
  14. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  15. Garofalo C, Russo P, Beneduce L, Massa S, Spano G, Capozzi V (2016a) Non-Saccharomyces biodiversity in wine and the ‘microbial terroir’: a survey on Nero di Troia wine from the Apulian region, Italy. Ann Microbiol 66:143–150. doi: 10.1007/s13213-015-1090-5 CrossRefGoogle Scholar
  16. Garofalo C, Tristezza M, Grieco F, Spano G, Capozzi V (2016b) From grape berries to wine: population dynamics of cultivable yeasts associated to “Nero di Troia” autochthonous grape cultivar. World J Microbiol Biotechnol 32:59. doi: 10.1007/s11274-016-2017-4 CrossRefPubMedGoogle Scholar
  17. Guzzon R, Widmann G, Settanni L, Malacarne M, Francesca N, Larcher R (2011) Evolution of yeast populations during different biodynamic winemaking processes. S Afr J Enol Vitic 32:242–250Google Scholar
  18. International Organization for Standardization (ISO) (1997) ISO 3591:1977. Sensory analysis—Apparatus—Wine-tasting glassGoogle Scholar
  19. Jolly NP, Varela C, Pretorius IS (2014) Not your ordinary yeast: non-Saccharomyces yeasts in wine production uncovered. FEMS Yeast Res 14:215–237. doi: 10.1111/1567-1364.12111 CrossRefPubMedGoogle Scholar
  20. Laghi L, Versari A, Marcolini E, Parpinello GP (2014) Metabonomic investigation by 1H-NMR to discriminate between red wines from organic and biodynamic grapes. Food Nutr Sci 5:52–59. doi: 10.4236/fns.2014.51007 CrossRefGoogle Scholar
  21. Lane JH, Eynon L (1923) Determination of reducing sugars by Fehling’s solution with methylene blue indicator. J Soc Chem Ind 42:32–37CrossRefGoogle Scholar
  22. Lawless HT, Heymann H (2010) Sensory evaluation of food: principles and practices. Chapman and Hall, New YorkCrossRefGoogle Scholar
  23. Loira I, Morata A, Comuzzo P, Callejo MJ, González C, Calderón F, Suárez-Lepe JA (2015) Use of Schizosaccharomyces pombe and Torulaspora delbrueckii strains in mixed and sequential fermentations to improve red wine sensory quality. Food Res Int 76:325–333. doi: 10.1016/j.foodres.2015.06.030 CrossRefGoogle Scholar
  24. Martins G, Miot-Sertier C, Lauga B, Claisse O, Lonvaud-Funel A, Soulas G, Masneuf-Pomarède I (2012) Grape berry bacterial microbiota: Impact of the ripening process and the farming system. Int J Food Microbiol 158:93–100. doi: 10.1016/j.ijfoodmicro.2012.06.013 CrossRefPubMedGoogle Scholar
  25. Martins G, Vallance J, Mercier A, Albertin W, Stamatopoulos P, Rey P, Lonvaud A, Masneuf-Pomarède I (2014) Influence of the farming system on the epiphytic yeasts and yeast-like fungi colonizing grape berries during the ripening process. Int J Food Microbiol 177:21–28. doi: 10.1016/j.ijfoodmicro.2014.02.002 CrossRefPubMedGoogle Scholar
  26. Muñoz-Bernal E, Rodríguez ME, Benítez P, Fernández-Acero FJ, Rebordinos L, Cantoral JM (2013) Molecular analysis of red wine yeast diversity in the Ribera del Duero D.O. (Spain) area. Arch Microbiol 195:297–302. doi: 10.1007/s00203-013-0872-z CrossRefPubMedGoogle Scholar
  27. Nisiotou AA, Nychas GJE (2007) Yeast populations residing on healthy or Botrytis-infected grapes from a vineyard in Attica, Greece. Appl Environ Microbiol 73:2765–2768. doi: 10.1128/AEM.01864-06 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Nuñez-Guerrero ME, Páez-Lerma JB, Rutiaga-Quiñones OM, González-Herrera SM, Soto-Cruz NO (2016) Performance of mixtures of Saccharomyces and non-Saccharomyces native yeasts during alcoholic fermentation of Agave duranguensis juice. Food Microbiol 54:91–97. doi: 10.1016/ CrossRefGoogle Scholar
  29. Parpinello GP, Rombolà AD, Simoni M, Versari A (2015) Chemical and sensory characterisation of Sangiovese red wines: comparison between biodynamic and organic management. Food Chem 167:145–152. doi: 10.1016/j.foodchem.2014.06.093 CrossRefPubMedGoogle Scholar
  30. Patrignani F, Ndagijimana M, Belletti N, Gardini F, Vernocchi P, Lanciotti R (2012) Biogenic amines and ethyl carbamate in Primitivo wine: survey of their concentrations in commercial products and relationship with the use of malolactic starter. J Food Prot 75:591–596. doi: 10.4315/0362-028X.JFP-11-311 CrossRefPubMedGoogle Scholar
  31. Patrignani F, Tabanelli G, Siroli L, Gardini F, Lanciotti R (2013) Combined effects of high pressure homogenization treatment and citral on microbiological quality of apricot juice. Int J Food Microbiol 160:273–281. doi: 10.1016/j.ijfoodmicro.2012.10.021 CrossRefPubMedGoogle Scholar
  32. Patrignani F, Chinnici F, Serrazanetti DI, Vernocchi P, Ndagijimana M, Riponi C, Lanciotti R (2016) Production of volatile and sulfur compounds by 10 Saccharomyces cerevisiae strains inoculated in Trebbiano must. Front Microbiol 7:243. doi: 10.3389/fmicb.2016.00243 PubMedPubMedCentralGoogle Scholar
  33. Pérez-Nevado F, Albergaria H, Hogg T, Girio F (2006) Cellular death of two non-Saccharomyces wine-related yeasts during mixed fermentations with Saccharomyces cerevisiae. Int J Food Microbiol 108:336–345PubMedGoogle Scholar
  34. Pretorius IS (2000) Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16:675–729CrossRefPubMedGoogle Scholar
  35. Rainieri S, Pretorius IS (2000) Selection and improvement of wine yeasts. Ann Microbiol 50:15–31Google Scholar
  36. Ranjard L, Echairi A, Nowak V, Lejon DPH, Nouaïm R, Chaussod R (2006) Field and microcosm experiments to evaluate the effects of agricultural Cu treatment on the density and genetic structure of microbial communities in two different soils. FEMS Microbiol Ecol 58:303–315CrossRefPubMedGoogle Scholar
  37. Reeve JR, Carpenter-Boggs L, Reganold JP, York AL, McGourty G, McCloskey LP (2005) Soil and winegrape quality in biodynamically and organically managed vineyards. Am J Enol Vitic 56:367–376Google Scholar
  38. Ripper M, Schmitt E (1896) Zeitschrift fach XXXV, 232Google Scholar
  39. Rocha S, Ramalheira V, Barros A, Delgadillo I, Coimbra MA (2001) Headspace solid phase microextraction (SPME) analysis of flavor compounds in wines. Effect of the matrix volatile composition in the relative response factors in a wine model. J Agric Food Chem 49:5142–5151CrossRefPubMedGoogle Scholar
  40. Romano P, Suzzi G, Comi G, Zironi R, Maifreni M (1997) Glycerol and other fermentation products of apiculate wine yeasts. J Appl Microbiol 82:615–618CrossRefPubMedGoogle Scholar
  41. Romano P, Fiore C, Paraggio M, Caruso M, Capece A (2003) Function of yeast species and strains in wine flavour. Int J Food Microbiol 86:169–180. doi: 10.1016/S0168-1605(03)00290-3 CrossRefPubMedGoogle Scholar
  42. Rosi I, Domizio P, Fia G, Agnoletto R (2000) Biodiversità della popolazione di lieviti presente nel corso della fermentazione di mosti di uve Sangiovese. Dissertation, Simposio Internazionale Il SangioveseGoogle Scholar
  43. Schuller D, Cardoso F, Sousa S, Gomes P, Gomes AC, Santos MAS, Casal M (2012) Genetic diversity and population structure of Saccharomyces cerevisiae strains isolated from different grape varieties and winemaking regions. PLoS One 7:e32507. doi: 10.1371/journal.pone.0032507 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Spaccini R, Mazzei P, Squartini A, Giannattasio M, Piccolo A (2012) Molecular properties of a fermented manure preparation used as field spray in biodynamic agriculture. Environ Sci Pollut Res Int 19:4214–4225. doi: 10.1007/s11356-012-1022-x CrossRefPubMedGoogle Scholar
  45. Tabanelli G, Montanari C, Grazia L, Lanciotti R, Gardini F (2013) Effects of aw at packaging time and atmosphere composition on aroma profile, biogenic amine content and microbiological features of dry fermented sausages. Meat Sci 94:177–186. doi: 10.1016/j.meatsci.2013.01.018 CrossRefPubMedGoogle Scholar
  46. Tassoni A, Tango N, Ferri M (2014) Polyphenol and biogenic amine profiles of Albana and Lambrusco grape berries and wines obtained following different agricultural and oenological practices. Food Nutr Sci 5:8–16. doi: 10.4236/fns.2014.51002 CrossRefGoogle Scholar
  47. Tofalo R, Torriani S, Chaves-López C, Martuscelli M, Paparella A, Suzzi G (2007) A survey of Saccharomyces populations associated with wine fermentations from the Apulia region (South Italy). Ann Microbiol 57:545–552CrossRefGoogle Scholar
  48. Tofalo R, Perpetuini G, Schirone M, Fasoli G, Aguzzi I, Corsetti A, Suzzi G (2013) Biogeographical characterization of Saccharomyces cerevisiae wine yeast by molecular methods. Front Microbiol 4:166–179. doi: 10.3389/fmicb.2013.00166 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Torrea D, Ancín A (2002) Content of biogenic amines in a Chardonnay wine obtained through spontaneous and inoculated fermentations. J Agric Food Chem 50:4895–4899CrossRefPubMedGoogle Scholar
  50. Tristezza M, Tufariello M, Capozzi V, Spano G, Mita G, Grieco F (2016) The oenological potential of Hanseniaspora uvarum in simultaneous and sequential co-fermentation with Saccharomyces cerevisiae for industrial wine production. Front Microbiol 7:1–14. doi: 10.3389/fmicb.2016.00670 CrossRefGoogle Scholar
  51. Ugliano M, Henschke PA (2009) Yeasts and wine flavour. In: Moreno-Arribas V, Polo MC (eds) Wine chemistry and biochemistry, chapter 8D. Springer, New York, pp 313–392CrossRefGoogle Scholar
  52. Valero E, Cambon B, Schuller D, Casal M, Dequin S (2007) Biodiversity of Saccharomyces yeast strains from grape berries of wine-producing areas using starter commercial yeasts. FEMS Yeast Res 7:317–329CrossRefPubMedGoogle Scholar
  53. Verginer M, Siegmund B, Cardinale M, Müller H, Choi Y, Míguez CB (2010) Monitoring the plant epiphyte Methylobacterium extorquens DSM 21961 by real-time PCR and its influence on the strawberry flavor. FEMS Microbiol Ecol 74:136–145. doi: 10.1111/j.1574-6941.2010.00942.x CrossRefPubMedGoogle Scholar
  54. Vernocchi P, Ndagijimana M, Serrazanetti DI, López CC, Fabiani A, Gardini F, Guerzoni ME, Lanciotti R (2011) Use of Saccharomyces cerevisiae strains endowed with beta-glucosidase activity for the production of Sangiovese wine. World J Microbiol Biotechnol 27:1423–1433. doi: 10.1007/s11274-010-0594-1 CrossRefPubMedGoogle Scholar
  55. Vernocchi P, Patrignani F, Ndagijimana M, Chaves Lopez C, Suzzi G, Gardini F, Lanciotti R (2015) Trebbiano wine produced by using Saccharomyces cerevisiae strains endowed with β-glucosidase activity. Ann Microbiol 65:1565–1571. doi: 10.1007/s13213-014-0995-8 CrossRefGoogle Scholar
  56. Viana F, Gil JV, Genovés S, Vallés S, Manzanares P (2008) Rational selection of non-Saccharomyces wine yeasts for mixed starters based on ester formation and enological traits. Food Microbiol 25:778–785. doi: 10.1016/ CrossRefPubMedGoogle Scholar
  57. Whiton RS, Zoecklein BW (2002) Determination of ethyl carbamate in wine by solid-phase microextraction and gas chromatography/mass spectrometry. Am J Enol Vitic 53:60–63Google Scholar
  58. Zott K, Miot-Sertier C, Claisse O, Lonvaud-Funel A, Masneuf-Pomarede I (2008) Dynamics and diversity of non-Saccharomyces yeasts during the early stages in winemaking. Int J Food Microbiol 125:197–203. doi: 10.1016/j.ijfoodmicro.2008.04.001 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg and the University of Milan 2016

Authors and Affiliations

  • Francesca Patrignani
    • 1
    • 2
  • Chiara Montanari
    • 2
  • Diana I. Serrazanetti
    • 2
  • Giacomo Braschi
    • 1
  • Pamela Vernocchi
    • 3
  • Giulia Tabanelli
    • 2
  • Giuseppina P. Parpinello
    • 1
    • 2
  • Andrea Versari
    • 1
    • 2
  • Fausto Gardini
    • 1
    • 2
  • Rosalba Lanciotti
    • 1
    • 2
    Email author
  1. 1.Department of Agricultural and Food SciencesUniversity of BolognaCesenaItaly
  2. 2.Interdepartmental Center for Industrial ResearchUniversity of BolognaCesenaItaly
  3. 3.Parasitology Unit, Department of Laboratory MedicineBambino Gesù Children’s Hospital, IRCCSRomeItaly

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