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Interaction between Oenococcus oeni and Lactobacillus hilgardii isolated from wine. Modification of available nitrogen and biogenic amine production

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Abstract

During the mixed culture of Lactobacillus hilgardii 5w, a common spoilage wine bacteria and Oenococcus oeni X2L, an amensalistic growth response of the malolactic bacteria was produced due to a competition for nitrogenous nutrients, mainly peptides. Arginine was fully consumed and peptide concentration diminished 60% with respect to both pure cultures at the end of exponential growth. Histamine release increased 34% with respect to L. hilgardii single culture. Under the poor nutritional conditions present during winemaking, L. hilgardii could increase histamine production and adversely affect malolactic fermentation conducted by O. oeni and hence the quality of the final product.

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References

  • Alberto MR, Arena ME, Manca de Nadra MC (2002) A comparative survey of two analytical methods for identification and quantification of biogenic amines. Food Control 13:125–129

    Article  CAS  Google Scholar 

  • Aredes Fernández PA, Manca de Nadra MC (2004) Amino acids profile in pure and mixed culture of wine lactic acid bacteria. Biocell 28:69

    Google Scholar 

  • Aredes Fernández PA, Manca de Nadra MC (2006) Growth response and modifications of organic nitrogen compounds in pure and mixed cultures of lactic acid bacteria from wine. Curr Microbiol 52:86–91

    Article  Google Scholar 

  • Aredes Fernández PA, Saguir FM, Manca de Nadra MC (2004) Effect of dipeptides on the growth of Oenococcus oeni in synthetic medium deprived of amino acids. Curr Microbiol 49:361–365

    Article  PubMed  Google Scholar 

  • Arena ME, Manca de Nadra MC (2001) Biogenic amine production by Lactobacillus. J Appl Microbiol 90:158–162

    Article  CAS  PubMed  Google Scholar 

  • Arena ME, Manca de Nadra MC (2005) Influence of ethanol and low pH on arginine and citrulline metabolism in lactic acid bacteria from wine. Res Microbiol 156:658–864

    Article  Google Scholar 

  • Arena ME, Manca de Nadra MC, Muñoz R (2002) The arginine deiminase pathway in the wine lactic acid bacterium Lactobacillus hilgardii X1B: structural and functional study of the arcABC genes. Gene 13:61–66

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Doi E, Shibata D, Matoba T (1981) Modified colorimetric ninhydrin methods for peptidase assay. Anal Biochem 118:173–184

    Article  CAS  PubMed  Google Scholar 

  • Farias ME, Manca de Nadra MC (2000) Purification and partial characterization of Oenococcus oeni exoprotease. FEMS Microbiol Lett 185:263–266

    Article  CAS  PubMed  Google Scholar 

  • Farías ME, Rollán GC, Strasser de Saad AM, Manca de Nadra MC (1993) Histidine decarboxylase activity in lactic acid bacteria from wine. J Int Sci Vigne Vin 27:191–199

    Google Scholar 

  • Farías ME, Manca de Nadra MC, Rollán GC, Strasser de Saad AM (1995) Histidine decarboxylase production by Lactobacillus hilgardii: effect of organic acids. Curr Microbiol 31:15–18

    Article  Google Scholar 

  • Farías ME, Rollan GC, Manca de Nadra MC (1996) Influence of nutritional factors on the protease production by Leuconostoc oenos from wine. J Appl Bacteriol 81:398–402

    Google Scholar 

  • Feuillat M, Guilloux-Benatier M, Gerbaux V (1985) Essais d’activation de la fermentation malolactique dans les vins. Sci Aliments 5:103–122

    CAS  Google Scholar 

  • García-Ruiz A, Bartolomé B, Cueva C, Martín-Álvarez PJ, Moreno-Arribas MV (2009) Inactivation of oenological lactic acid bacteria (Lactobacillus hilgardii and Pediococcus pentosaceus) by wine phenolic compounds. J App Microbiol 107:1042–1053

    Article  Google Scholar 

  • Herbert P, Cabrita MJ, Ratola N, Laureano O, Alves A (2006) Relationship between biogenic amines and free amino acid contents of wines and musts from Alentejo (Portugal). J Environ Sci Health B 41:1171–1186

    CAS  PubMed  Google Scholar 

  • Izquierdo Cañas PM, García Romero E, Gómez Alonso S, Fernández González M, Palop Herreros MLL (2008) Amino acids and biogenic amines during spontaneous malolactic fermentation in Tempranillo red wines. J Food Compos Anal 21:731–735

    Article  Google Scholar 

  • Konings WN (2002) The cell membrane and the struggle for life of lactic acid bacteria. Antonie Van Leeuwenhoek 82:3–27

    Article  CAS  PubMed  Google Scholar 

  • Konings WN (2006) Microbial transport: adaptations to natural environments. Antonie Van Leeuwenhoek 90:325–342

    Article  CAS  PubMed  Google Scholar 

  • Manca de Nadra MC, Aredes Fernández PA (2008) Modification of nitrogenous compounds by lactic acid bacteria interactions. In: Manca de Nadra MC (ed) Nitrogen compounds metabolism by lactic acid bacteria. Research Signpost, India, pp 169–191

    Google Scholar 

  • Manca de Nadra MC, Strasser de Saad AM (1987) Evolution of lactic acid bacteria during the different stages of vinification of Cafayate (Argentine) wines. Micr Alim Nutr 5:235–240

    CAS  Google Scholar 

  • Manca de Nadra MC, Farías ME, Moreno-Arribas MV, Pueyo E, Polo MC (1997) Proteolytic activity of Leuconostoc oenos. effect of proteins and polypeptides from white wine. FEMS Microbiol Lett 150:135–139

    Article  CAS  Google Scholar 

  • Manca de Nadra MC, Farías ME, Moreno-Arribas MV, Pueyo E, Polo MC (1999) A proteolytic effect of Oenococcus oeni on the nitrogenous macromolecular fraction of red wine. FEMS Microbiol Lett 174:41–47

    Article  Google Scholar 

  • Manca de Nadra MC, Farías ME, Pueyo E, Polo MC (2005) Protease activity of Oenococcus oeni viable cells on red wine nitrogenous macromolecular fraction in presence of SO2 and ethanol. Food Control 16:851–854

    Article  CAS  Google Scholar 

  • Manca de Nadra MC, Farías ME, Aredes Fernández PA (2006) Interacciones microbianas. In: Torres Vitela MR, Castillo Ayala A (eds) Microbiología de los alimentos. Universidad de Guadalajara, México, pp 515–533

    Google Scholar 

  • Mazzoli R, Lamberti C, Coisson JD, Purrotti M, Arlorio M, Giuffrida MG, Giunta C, Pessione E (2009) Influence of ethanol, malate and arginine on histamine production of Lactobacillus hilgardii isolated from an Italian red wine. Amino Acids 36:81–89

    Article  CAS  PubMed  Google Scholar 

  • Nuñez de Kairuz MS, Olazábal ME, Oliver G, Pesce de Ruiz Holgado AA, Massa E, Farías RN (1988) Fatty acid dependent hydrogen peroxide production in Lactobacillus. Biochem Biophys Res Commun 15:113–121

    Article  Google Scholar 

  • Osborne JP, Edwards CG (2005) Bacteria important during winemaking. Adv Food Nutr Res 50:139–177

    Article  CAS  PubMed  Google Scholar 

  • Remize F, Gaudin A, Kong Y, Guzzo J, Alexandre H, Krieger S, Guilloux-Benatier M (2006) Oenococcus oeni preference for peptides: qualitative and quantitative analysis of nitrogen assimilation. Arch Microbiol 185:459–469

    Article  CAS  PubMed  Google Scholar 

  • Ribéreau-Gayon P, Dubordieu D, Doneche B, Lonvaud A (1998) Traité d′œnologie: 1- Microbiologie du Vin, Vinifications. Dunod, Paris

    Google Scholar 

  • Ritt J-F, Guilloux-Benatier M, Guzzo J, Alexandre H, Remize F (2008) Oligopeptide assimilation and transport by Oenococcus oeni. J Appl Microbiol 104:573–580

    CAS  PubMed  Google Scholar 

  • Rodríguez AV, Manca de Nadra MC (1995) Production of hydrogen peroxide by Lactobacillus hilgardii and its effect on Leuconostoc oenos growth. Curr Microbiol 30:23–25

    Article  Google Scholar 

  • Rollan GC, Farias ME, Manca de Nadra MC (1993) Protease production by Leuconostos oenos strains isolated from wine. World J Microbiol Biotechnol 9:587–589

    Article  CAS  Google Scholar 

  • Soufleros EH, Bouloumpasi E, Zotou A, Loukou Z (2007) Determination of biogenic amines in Greek wines by HPLC and ultraviolet detection after dansylation and examination of factors affecting their presence and concentration. Food Chem 101:704–716

    Article  CAS  Google Scholar 

  • Strasser de Saad AM, Manca de Nadra MC (1987) Isolation and identification of lactic acid bacteria from Cafayate (Argentina) wines. Micr Alim Nutr 5:45–49

    Google Scholar 

  • Suzzi G, Gardini F (2003) Biogenic amines in dry fermented sausages: a review. Int J Food Microbiol 88:41–54

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was financially supported by Consejo Nacional de Investigaciones Científicas y Técnicas (PIP CONICET 6495), Consejo de Investigaciones de la Universidad Nacional de Tucumán (CIUNT 26/D436-1) and Agencia Nacional de Promoción Científica y Tecnológica (PICT 32867) Argentina.

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Authors and Affiliations

  1. Centro de Referencia para Lactobacillus (CERELA), Chacabuco 145, Tucumán, Argentina

    Pedro A. Aredes Fernández, Marta E. Farías & María C. Manca de Nadra

  2. Facultad de Bioquímica, Química y Farmacia, Universidad Nacional de Tucumán, Ayacucho 491, Tucumán, 4000, Argentina

    Marta E. Farías & María C. Manca de Nadra

Authors
  1. Pedro A. Aredes Fernández
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  2. Marta E. Farías
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  3. María C. Manca de Nadra
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Correspondence to Marta E. Farías.

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Aredes Fernández, P.A., Farías, M.E. & de Nadra, M.C.M. Interaction between Oenococcus oeni and Lactobacillus hilgardii isolated from wine. Modification of available nitrogen and biogenic amine production. Biotechnol Lett 32, 1095–1102 (2010). https://doi.org/10.1007/s10529-010-0260-6

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  • DOI: https://doi.org/10.1007/s10529-010-0260-6

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