Skip to main content
SpringerLink
Log in

Antioxidant properties of wine lactic acid bacteria: Oenococcus oeni

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • 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 97:809–817

    Article  CAS  PubMed  Google Scholar 

  • 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 163:166–170

    Article  CAS  PubMed  Google Scholar 

  • 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 14:809–813

    Article  CAS  PubMed  Google Scholar 

  • 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 33:359–364

    Article  PubMed  Google Scholar 

  • 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 33:282–291

    Article  CAS  PubMed  Google Scholar 

  • Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76

    Article  CAS  PubMed  Google Scholar 

  • Buettner GR (1990) Use of ascorbate as test for catalytic metals in sample buffers. Methods Enzymol 186:125–127

    CAS  PubMed  Google Scholar 

  • 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 63:1369–1376

    CAS  PubMed  Google Scholar 

  • 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 75:4887–4891

    Article  PubMed  Google Scholar 

  • 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 133:862–874

    Article  PubMed  Google Scholar 

  • 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 13:236–243

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 140:136–145

    Article  PubMed  Google Scholar 

  • 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 44:220–225

    Article  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1–14

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jensen H, Grimmer S, Naterstad K, Axelsson L (2012) In vitro testing of commercial and potential probiotic lactic acid bacteria. Int J Food Microbiol 153:216–222

    Article  PubMed  Google Scholar 

  • 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 145:1245–1251

    Article  CAS  PubMed  Google Scholar 

  • Kavitha V, Palanivelu K (2004) The role of ferrous ion in Fenton and photo-Fenton processes for the degradation of phenol. Chemosphere 55:1235–1243

    Article  CAS  PubMed  Google Scholar 

  • 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 14:2029–2036

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 72:215–224

    Article  CAS  PubMed  Google Scholar 

  • 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–m391

    Article  CAS  Google Scholar 

  • Li H, Zhang C, Liu Y (2006) Species attribution and distinguishing strains of Oenococcus oeni isolated from Chinese wines. World J Microbiol Biotechnol 22:515–518

    Article  CAS  Google Scholar 

  • Lin MY, Chang FJ (2000) Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 45:1617–1622

    Article  CAS  PubMed  Google Scholar 

  • Lin MY, Yen CL (1999) Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47:1460–1466

    Article  CAS  PubMed  Google Scholar 

  • 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 56:315–321

    Article  CAS  PubMed  Google Scholar 

  • Mikelsaar M, Zilmer M (2009) Lactobacillus fermentum ME-3—an antimicrobial and antioxidative probiotic. Microbiol Ecol Health Dis 21:1–27

    Article  CAS  Google Scholar 

  • Oyaizu M (1986) Antioxidative activity of browning products of glucosamine fractionated by organic solvent and thin-layer chromatography. Nippon Shokuhin Kogyo Gakkaishi 35:771–775

    Article  Google Scholar 

  • Prisciandaro L, Geier M, Butler R, Cummins A, Howarth G (2009) Probiotics and their derivatives as treatments for inflammatory bowel disease. Inflamm Bowel Dis 15:1906–1914

    Article  PubMed  Google Scholar 

  • 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: 33–38

  • Rivera-Espinoza Y, Gallardo-Navarro Y (2010) Non-dairy probiotic products. Food Microbiol 27:1–11

    Article  PubMed  Google Scholar 

  • 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 70:2748–2755

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 4:22

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 56:285–294

    Article  PubMed  Google Scholar 

  • 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 98:2395–2413

    Article  CAS  PubMed  Google Scholar 

  • 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 29:1913–1922

    Article  PubMed  Google Scholar 

  • 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 36:895–904

    Article  CAS  Google Scholar 

  • 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 45:632–638

    Article  Google Scholar 

  • Wang H, Jin G, Li CX, Du LY, Li H (2010) Optimization of rapid specificity identification of Oenococcus oeni. China Brew 5:152–156

    Google Scholar 

  • 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 105:1266–1276

    Article  CAS  PubMed  Google Scholar 

  • Zúñiga M, Pardo I, Ferrer S (1993) An improved medium for distinguishing between homofermentative and heterofermentative lactic acid bacteria. Int J Food Microbiol 18:37–42

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

  1. College of Food Science and Engineering, Northwest A&F University, Yangling, Shaanxi, 712100, China

    Jing Su

  2. College of Enology, Northwest A&F University, Yangling, Shaanxi, 712100, China

    Tao Wang, Ying-Ying Li, Jing Li, Yu Zhang, Yun Wang, Hua Wang & Hua Li

  3. Shaanxi Engineering Research Center for Viti-Viniculture, Yangling, Shaanxi, 712100, China

    Hua Li

  4. Heyang Experimental and Demonstrational Stations for Grape, Weinan, Shaanxi, 715300, China

    Hua Li

Authors
  1. Jing Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ying-Ying Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hua Wang or Hua Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Su, J., Wang, T., Li, YY. et al. Antioxidant properties of wine lactic acid bacteria: Oenococcus oeni . Appl Microbiol Biotechnol 99, 5189–5202 (2015). https://doi.org/10.1007/s00253-015-6425-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-015-6425-4

Keywords

Search

Navigation