Applied Microbiology and Biotechnology

, Volume 99, Issue 12, pp 5189–5202 | Cite as

Antioxidant properties of wine lactic acid bacteria: Oenococcus oeni

  • Jing Su
  • Tao Wang
  • Ying-Ying Li
  • Jing Li
  • Yu Zhang
  • Yun Wang
  • Hua WangEmail author
  • Hua LiEmail author
Applied microbial and cell physiology


The most prominent trait of wine lactic acid bacteria (LAB) is their capacity to cope with a hostile environment. However, wine-derived LAB may confer inherent probiotic properties that have not been explored. In this study, the antioxidant activities of 19 strains of Oenococcus oeni were measured in vitro. The results suggested that the antioxidative parameters were widely dispersed, irrespective of the evaluation methods used, which indicated that antioxidative properties depended on the strain and culture medium. The antioxidant mechanisms of O. oeni could be assigned to the 2,2-diphenyl-1-picrylhydrazyl (DPPH) scavenging ability, reactive oxygen species (ROS) scavenging ability, iron ion chelation (FE), glutathione system, ferric reducing ability of plasma (FRAP), reduction activity (RA), inhibition of ascorbic oxidation (TAA), and linoleic acid oxidation (TLA) abilities. Moreover, most of the O. oeni strains exhibited good survival abilities at low pH values (pH 1.8), simulated intestine juice and bile salts (1 %), suggesting their good adaptation to gastrointestinal conditions and high bile resistance abilities. O. oeni SD-1e, SD-2gf, 31-DH, and SD-2d with promising potential probiotic characteristics were segregated by the principal component analysis (PCA). O. oeni strains likely serve as defensive agents in the intestinal microbial ecosystem and overcome exogenous and endogenous oxidative stress. Although further studies are needed to elucidate the multiple mechanisms involved, the study reported herein confirms the effectiveness of O. oeni in the defense against in vitro oxidative stress.


Oenococcus oeni Antioxidant properties Principal component analysis Wine Probiotics 



The authors gratefully acknowledge the financial support of the National “Twelfth Five-Year” Plan for Science and Technology Support “Key Technology Research and Industry Demonstration of High Quality Fruit Wine” (2012BAD31B07). This work was also financially supported by the National Natural Science Foundation of China (Grant No. 31471708).


  1. Amaretti A, di Nunzio M, Pompei A, Raimondi S, Rossi M, Bordoni A (2013) Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities. Appl Microbiol Biotechnol 97:809–817CrossRefPubMedGoogle Scholar
  2. Apud GR, Rodríguez Vaquero MJ, Rollan G, Stivala MG, Aredes Fernández PA (2013a) Increase in antioxidant and antihypertensive peptides from Argentinean wines by Oenococcus oeni. Int J Food Microbiol 163:166–170CrossRefPubMedGoogle Scholar
  3. Apud GR, Stivala MG, Aredes Fernández PA, Rodríguez Vaquero MJ (2013b) Proteolytic activity of Oenococcus oeni enables the increase in antioxidant and antihypertensive activities from wine. Curr Pharm Biotechnol 14:809–813CrossRefPubMedGoogle Scholar
  4. Aredes Fernández PA, Stivala MG, Rodríguez Vaquero MJ, Farías ME (2011) Increase in antioxidant and antihypertensive activity by Oenococcus oeni in a yeast autolysis wine model. Biotechnol Lett 33:359–364CrossRefPubMedGoogle Scholar
  5. Argyri AA, Zoumpopoulou G, Karatzas KAG, Tsakalidou E, Nychas GJE, Panagou EZ, Tassou CC (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33:282–291CrossRefPubMedGoogle Scholar
  6. Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76CrossRefPubMedGoogle Scholar
  7. Buettner GR (1990) Use of ascorbate as test for catalytic metals in sample buffers. Methods Enzymol 186:125–127PubMedGoogle Scholar
  8. Charteris WP, Kelly PM, Morelli L, Collins JK (2000) Effect of conjugated bile salts on antibiotic susceptibility of bile salt-tolerant Lactobacillus and Bifidobacterium isolates. J Food Prot 63:1369–1376PubMedGoogle Scholar
  9. de Palencia PF, Werning ML, Sierra-Filardi E, Dueñas MT, Irastorza A, Corbí AL, López P (2009) Probiotic properties of the 2-substituted (1, 3)-beta-D-glucan-producing bacterium Pediococcus parvulus 2.6. Appl Environ Microbiol 75:4887–4891CrossRefPubMedGoogle Scholar
  10. Foligné B, Dessein R, Marceau M, Poiret S, Chamaillard M, Pot B, Simonet M, Daniel C (2007a) Prevention and treatment of colitis with Lactococcus lactis secreting the immunomodulatory Yersinia LcrV protein. Gastroenterology 133:862–874CrossRefPubMedGoogle Scholar
  11. Foligné B, Nutten S, Grangette C, Dennin V, Goudercourt D, Poiret S, Dewulf J, Brassart D, Mercenier A, Pot B (2007b) Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J Gastroenterol 13:236–243CrossRefPubMedCentralPubMedGoogle Scholar
  12. Foligné B, Dewulf J, Breton J, Claisse O, Lonvaud-Funel A, Pot B (2010) Probiotic properties of non-conventional lactic acid bacteria: Immunomodulation by Oenococcus oeni. Int J Food Microbiol 140:136–145CrossRefPubMedGoogle Scholar
  13. García-Ruiz A, González de Llano D, Esteban-Fernández A, Requena T, Bartolomé B, Moreno-Arribas MV (2014) Assessment of probiotic properties in lactic acid bacteria isolated from wine. Food Microbiol 44:220–225CrossRefPubMedGoogle Scholar
  14. Halliwell B, Gutteridge JMC (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1–14PubMedCentralPubMedGoogle Scholar
  15. Jensen H, Grimmer S, Naterstad K, Axelsson L (2012) In vitro testing of commercial and potential probiotic lactic acid bacteria. Int J Food Microbiol 153:216–222CrossRefPubMedGoogle Scholar
  16. Jobin MP, Garmyn D, Diviès C, Guzzo J (1999) Expression of the Oenococcus oeni trxA gene is induced by hydrogen peroxide and heat shock. Microbiology 145:1245–1251CrossRefPubMedGoogle Scholar
  17. Kavitha V, Palanivelu K (2004) The role of ferrous ion in Fenton and photo-Fenton processes for the degradation of phenol. Chemosphere 55:1235–1243CrossRefPubMedGoogle Scholar
  18. Kekkonen RA, Lummela N, Karjalainen H, Latvala S, Tynkkynen S, Järvenpää S, Kautiainen H, Julkunen I, Vapaatalo H, Korpela R (2008) Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J Gastroenterol 14:2029–2036CrossRefPubMedCentralPubMedGoogle Scholar
  19. Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 72:215–224CrossRefPubMedGoogle Scholar
  20. Lee J, Hwang KT, Chung MY, Cho DH, Park CS (2005) Resistance of Lactobacillus casei KCTC 3260 to reactive oxygen species (ROS): role for a metal ion chelating effect. J Food Sci 70:m388–m391CrossRefGoogle Scholar
  21. Li H, Zhang C, Liu Y (2006) Species attribution and distinguishing strains of Oenococcus oeni isolated from Chinese wines. World J Microbiol Biotechnol 22:515–518CrossRefGoogle Scholar
  22. Lin MY, Chang FJ (2000) Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 45:1617–1622CrossRefPubMedGoogle Scholar
  23. Lin MY, Yen CL (1999) Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47:1460–1466CrossRefPubMedGoogle Scholar
  24. Mathara JM, Schillinger U, Kutima PM, Mbugua SK, Guigas C, Franz C, Holzapfel WH (2008) Functional properties of Lactobacillus plantarum strains isolated from Maasai traditional fermented milk products in Kenya. Curr Microbiol 56:315–321CrossRefPubMedGoogle Scholar
  25. Mikelsaar M, Zilmer M (2009) Lactobacillus fermentum ME-3—an antimicrobial and antioxidative probiotic. Microbiol Ecol Health Dis 21:1–27CrossRefGoogle Scholar
  26. Oyaizu M (1986) Antioxidative activity of browning products of glucosamine fractionated by organic solvent and thin-layer chromatography. Nippon Shokuhin Kogyo Gakkaishi 35:771–775CrossRefGoogle Scholar
  27. Prisciandaro L, Geier M, Butler R, Cummins A, Howarth G (2009) Probiotics and their derivatives as treatments for inflammatory bowel disease. Inflamm Bowel Dis 15:1906–1914CrossRefPubMedGoogle Scholar
  28. Rauhut D, Gawron-Scibek M, Beisert B, Kondzior M, Schwarz R, Kürbel H, Grossmann M, Krieger S (2004) Impact of S-containing amino acids and glutathione on growth of Oenococcus oeni and malolactic fermentation. In: Proceedings of LES XVIe Entretiens Scientifiques Lallemand, Porto, May 4–5: 33–38Google Scholar
  29. Rivera-Espinoza Y, Gallardo-Navarro Y (2010) Non-dairy probiotic products. Food Microbiol 27:1–11CrossRefPubMedGoogle Scholar
  30. Silveira MG, Baumgärtner M, Rombouts FM, Abee T (2004) Effect of adaptation to ethanol on cytoplasmic and membrane protein profiles of Oenococcus oeni. Appl Environ Microbiol 70:2748–2755CrossRefPubMedCentralPubMedGoogle Scholar
  31. Songisepp E, Kals J, Kullisaar T, Mändar R, Hütt P, Zilmer M, Mikelsaar M (2005) Evaluation of the functional efficacy of an antioxidative probiotic in healthy volunteers. Nutr J 4:22CrossRefPubMedCentralPubMedGoogle Scholar
  32. Spyropoulos BG, Misiakos EP, Fotiadis C, Stoidis CN (2011) Antioxidant properties of probiotics and their protective effects in the pathogenesis of radiation-induced enteritis and colitis. Dig Dis Sci 56:285–294CrossRefPubMedGoogle Scholar
  33. Su J, Wang T, Wang Y, Li YY, Li H (2014) The use of lactic acid-producing, malic acid-producing, or malic acid-degrading yeast strains for acidity adjustment in the wine industry. Appl Microbiol Biotechnol 98:2395–2413CrossRefPubMedGoogle Scholar
  34. Turchi B, Mancini S, Fratini F, Pedonese F, Nuvoloni R, Bertelloni F, Ebani VV, Cerri D (2013) Preliminary evaluation of probiotic potential of Lactobacillus plantarum strains isolated from Italian food products. World J Microbiol Biotechnol 29:1913–1922CrossRefPubMedGoogle Scholar
  35. Vinderola CG, Reinheimer JA (2003) Lactic acid starter and probiotic bacteria: a comparative “in vitro” study of probiotic characteristics and biological barrier resistance. Food Res Int 36:895–904CrossRefGoogle Scholar
  36. von Gadow A, Joubert E, Hansmann CF (1997) Comparison of the antioxidant activity of aspalathin with that of other plant phenols of rooibos tea (Aspalathus linearis), α-tocopherol, BHT, and BHA. J Agric Food Chem 45:632–638CrossRefGoogle Scholar
  37. Wang H, Jin G, Li CX, Du LY, Li H (2010) Optimization of rapid specificity identification of Oenococcus oeni. China Brew 5:152–156Google Scholar
  38. Zanoni S, Pompei A, Cordisco L, Amaretti A, Rossi M, Matteuzzi D (2008) Growth kinetics on oligo- and polysaccharides and promising features of three antioxidative potential probiotic strains. J Appl Microbiol 105:1266–1276CrossRefPubMedGoogle Scholar
  39. Zúñiga M, Pardo I, Ferrer S (1993) An improved medium for distinguishing between homofermentative and heterofermentative lactic acid bacteria. Int J Food Microbiol 18:37–42CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.College of Food Science and EngineeringNorthwest A&F UniversityYanglingChina
  2. 2.College of EnologyNorthwest A&F UniversityYanglingChina
  3. 3.Shaanxi Engineering Research Center for Viti-VinicultureYanglingChina
  4. 4.Heyang Experimental and Demonstrational Stations for GrapeWeinanChina

Personalised recommendations