Abstract
Wine, like other fermented foods, may contain biogenic amines produced by lactic acid bacteria via amino acids decarboxylation. The most relevant amines from the toxicological standpoint are histamine and tyramine. The complexity of fermented substrates makes it difficult to suggest a priori how variables can modulate amine production. Lactobacillus hilgardii ISE 5211 was isolated from an Italian red wine. Besides producing lactate from malate, this strain is also able to convert arginine to ornithine and histidine to histamine. In the present investigation we studied the influence of malate, arginine and ethanol on histamine accumulation by L. hilgardii ISE 5211. Ethanol concentrations above 13% inhibit both histamine accumulation and bacterial growth; concentrations below 9% affect neither growth nor histamine production. However, an ethanol concentration of 11% allows a low but continuous accumulation of histamine to occur. Arginine also delays histamine accumulation, while malate appears to have no effect on histidine–histamine conversion.
Similar content being viewed by others
References
Anli ER, Vural N, Yilmaz S, Vural YH (2004) The determination of biogenic amines in Turkish red wines. J Food Composit Anal 17:53–62
Arena ME, Manca de Nadra MC (2001) Biogenic amine production by Lactobacillus. J Appl Microbiol 90(2):158–162
Bauza T, Teissedre PL (1995) Formation of biogenic amines as criteria for the selection of wine yeasts. Bull Off Int du Vin 68:42–67
Bodmer S, Imark C, Kneubuhl M (1999) Biogenic amines in foods: histamine and food processing. Inflamm Res 48(6):296–300
Bover-Cid S, Hugas M, Izquierdo-Pulido M, Vidal-Carou MC (2001) Amino acid-decarboxylase activity of bacteria isolated from fermented pork sausages. Int J Food Microbiol 66:185–189
Brandolini V, Salzano G, Maietti A, Caruso M, Tedeschi P, Mazzotta D, Romano P (2002) Automated multiple development method for determination of glycerol produced by wine yeasts. World J Microbiol Biotechnol 18(5):481–485
Busto O, Guash J, Borrull F (1996) Biogenic amines in wine: a review of analytical methods. Int Sci de la vigne et du Vin 2:85–101
Coïsson D, Cerutti C, Travaglia F, Arlorio M (2004) Production of biogenic amines in “salamini italiani alla cacciatora PDO”. Meat Science 67:343–349
Coton E, Torlois S, Bertrand A, Lonvaud-Funel A (1999) Biogenic amines and wine lactic acid bacteria. Bull de L’OIV 815–816:22–34
Couto JA, Rozès N, Hogg T (1996) Ethanol-induced changes in the fatty acid composition of Lactobacillus hilgardii, its effects on plasma membrane fluidity and relationship with ethanol tolerance. J Appl Bacteriol 81:126–132
De Angelis M, Mariotti L, Rossi J, Servili M, Fox PF, Rollán G, Gobbetti M (2002) Arginine catabolism by sourdough lactic acid bacteria: purification and characterization of the arginine deiminase pathway enzymes from Lactobacillus sanfranciscensis CB1. Appl Environ Microbiol 68:6193–6201
Fleet GH (2003) Yeast interactions and wine flavour. Int J Food Microbiol 86:11–22
Gardini F, Zaccarelli A, Belletti N, Faustini F, Cavazza A, Martuscelli M, Mastrocola D, Suzzi G (2005) Factors influencing biogenic amine production by a strain of Oenococcus oeni in a model system. Food Control 16:609–616
Gerbaux V, Monamy C (2000) Biogenic amines in Burgundy wines. Contents and origin in wines, Revue Français d’Oenologie 183:25–28
Gerbaux V, Villa A, Monamy C, Bertrand A (1997) Use of lysozyme to inhibit malolactic fermentation and to stabilize wine after malolactic fermentation. Am J Enol Viticult 48(1):49–54
Gloria MBA, Watson BT, Simon-Sarkadi L, Daeschel MA (1998) A survey of biogenic amines in Oregon Pinot noir and Cabernet Sauvignon wines. Am J Enol Vitic 49:279–282
Gómez-Alonso S, Hermosín-Gutiérrez I, García-Romero E (2007) Simultaneous HPLC analysis of biogenic amines, amino acids and ammonium ion as aminoenone derivatives in wine and beer samples. J Agric Food Chem 55(3):608–613
Guerrini S, Mangani S, Granchi L, Vincenzini M (2002) Biogenic amine production by Oenococcus oeni. Curr Microbiol 44:374–378
Halasz A, Barath A, Simon-Sarkadi L, Holzapfel W (1994) Biogenic amines and their production by microorganisms in food. Trends Food Sci Technol 5:42–49
Hellman U, Wernstedt C, Gonez J, Heldin CH (1995) Improvement of an in-gel digestion procedure for the micropreparation of internal protein-fragments for amino-acid sequencing. Anal Biochem 224:451–455
Henschke PA, Jiranek V (1993) Yeasts-metabolism of nitrogen compounds. In: Fleet GH (ed) Wine microbiology and biotechnology. Harwood Academic Publishers, Chur, Switzerland, pp 77–164
Konings WN, Lolkema JS, Bolhuis M, Van Veen HW, Poolman B, Driessen AJ (1997) The role of transport processes in survival of lactic acid bacteria—energy transduction and multidrug resistance. Antonie van Leeuw 71:117–128
Lambrechts MG, Pretorius IS (2000) Yeast and its importance to wine aroma: a review. S Afr J Enol Vitic 21:97–129
Landete JM, Pardo I, Ferrer S (2006) Histamine, histidine, and growth-phase mediated regulation of the histidine decarboxylase gene in lactic acid bacteria isolated from wine. FEMS Microbiol Lett 260:84–90
Landete JM, De las Rivas B, Marcolbal A, Munoz R (2007) Molecular methods for the detection of biogenic amine-producing bacteria on food. Int J Food Microbiol 117:258–269
Lehtonen P (1996) Determination of amines and amino acids in wine—a review. Am J Enol Vitic 47:127–133
Leitao MC, Marques AP, San Romao MV (2005) A survey of biogenic amines in commercial Portuguese wines. Food Control 16:199–204
Liu S, Pritchard GG, Hardman MJ, Pilone GJ (1995) Occurrence af arginine deiminase pathway in arginine catabolism by wine lactic acid bacteria. Appl Environ Microbiol 61(1):310–316
Lonvaud-Funel A (1999) Lactic acid bacteria in the quality improvement and depreciation of wine. Antonie van Leeuwenhoek 76:317–331
Lonvaud-Funel A (2001) Biogenic amines in wines: role of lactic acid bacteria. FEMS Microbiology Letters 199:9–13
Lonvaud-Funel A, Joyeux A (1994) Histamine production by wine lactic acid bacteria: isolation of a histamine-producing strain of Leuconostoc oenos. J Appl Bacteriol 77:401–407
Lovaas E (1991) Antioxidative effects of polyamines. J Am Oil Chem Soc 68:353–358
Mangani S, Guerrini S, Granchi L, Vincenzini M (2005) Putrescine accumulation in wine: role of Oenococcus oeni. Curr Microbiol 51(1):6–10
Maynard LS, Schenker VJ (1962) Monoamine oxidase inhibition by ethanol in vitro. Nature 196:575–576
Moreno-Arribas V, Lonvaud-Funel A (1999) Tyrosine decarboxylase activity of Lactobacillus brevis IOEB 9809 isolated from wine and L. brevis ATCC 367. FEMS Microbiol Lett 180:55–60
Moreno-Arribas MV, Polo MC, Jourganes F, Munoz R (2003) Screening of biogenic amine production by lactic acid bacteria isolated from grape must and wine. Int J Food Microbiol 84:117–123
Moreno-Arribas V, Torlois S, Joyeux A, Bertrand A, Lonvaud-Funel A (2000) Isolation, properties and behaviour of tyramine-producing lactic acid bacteria from wine. J Appl Microbiol 88:584–593
Pappin DJ, Hojrup P, Bleasby AJ (1993) Rapid identification of proteins by peptide-mass fingerprinting. Curr Biol 3(6):327–332
Perrot L, Charpentier M, Charpentier C, Feuillat M, Chassagne D (2002) Yeast adapted to wine: nitrogen compounds released during induced autolysis in a model wine. J Ind Microbiol Biotechnol 29:134–139
Pessione E, Mazzoli R, Giuffrida MG, Lamberti C, Garcia-Moruno E, Barello C, Conti A, Giunta C (2005) A proteomic approach to studying biogenic amine producing lactic acid bacteria. Proteomics 5:687–689
Pozo-Bayon MA, G-Alegría E, Polo MC, Tenorio C, Martín-Alvarez PJ, Calvo de La Banda MT, Ruiz-Larrea F, Moreno-Arribas MV (2005) Wine volatile and amino acid composition after malolactic fermentation: effect of Oenococcus oeni and Lactobacillus plantarum starter cultures. J Agric Food Chem 53:8729–8735
Romano P, Caruso M, Capece A, Lipani G, Paraggio M, Fiore C (2003a) Metabolic diversity of Saccharomyces cerevisiae strains from spontaneously fermented grape musts. World J Microbiol Biotechnol 19:311–315
Romano P, Fiore C, Paraggio M, Caruso M, Capece A (2003b) Function of yeast species and strains in wine flavour. Int J Food Microbiol 86:169–180
Romero R, Sanchez-Vinas M, Gazquez D, Gracia B (2002) Characterization of selected Spanish table wine samples according to their biogenic amine content from liquid chromatographic determination. J Agr Food Chem 50(16):4713–4717
Sessa A, Desiderio MA, Perin A (1984) Effect of acute ethanol administration on diamine oxidase activity on the upper gastrointestinal tract of rat. Alcohol Clin Exp Res 8:185–190
Shalaby AR (1996) Significance of biogenic amines to food safety and human health. Food Res Int 26:675–690
Silla Santos MH (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29:213–231
Soufleros E, Barrios ML, Bertrand A (1998) Correlation between the content of biogenic amines and other wine compounds. Am J Enol Vitic 49:266–278
Taylor SL (1986) Histamine food poisoning: toxicology and clinical aspects. Crit Rev Toxicol 17:91–128
Teixeira H, Gonçalves MG, Rozès N, Ramos A, San Romão MV (2002) Lactobacillic acid accumulation in the plasma membrane of Oenococcus oeni: a response to ethanol stress? Microb Ecol 43:146–153
Ten Brink B, Damink C, Joosten HMLJ, Huis in’t Veld JHJ (1990) Occurrence and formation of biologically-active amines in foods. Int J Food Microbiol 11:73–84
Terrade N, Mira de Orduna R (2006) Impact of winemaking practices on arginine and citrulline metabolism during and after malolactic fermentation. J Appl Microbiol 101(2):406–411
Torrea D, Ancin C (2002) Content of biogenic Amines in a Chardonnay wine obtained through spontaneous and inoculated fermentations. J Agric Food Chem 50:4895–4899
Vidal-Carou MC, Ambatille-Espunyes A, Ulla-Ulla MC, Mariné-Font A (1990a) Histamine and tyramine in ish wines: their formation during the wine making process. Am J Enol Vitic 41:160–167
Vidal-Carou MC, Izquierdo-Pulido M, Martín-Morro M, Mariné-Font A, (1990b) Histamine and tyramine in meat products: relationship with meat spoilage. Food Chem 37:239–349
Vidal-Carou MC, Codony-Salcedo R, Mariné-Font A, (1991) Changes in the concentration of histamine and tyramine during wine spoilage at various temperatures. Am J Enol Vitic 42:145–149
Acknowledgments
This research work has been financed by grants from Regione Piemonte (CIPE 2004, Ricerca Sanitaria Finalizzata 2004) and MIUR. The authors gratefully acknowledge Emilia Garcia-Moruno for kindly supplying the ISE5211 strain.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mazzoli, R., Lamberti, C., Coisson, J.D. et al. Influence of ethanol, malate and arginine on histamine production of Lactobacillus hilgardii isolated from an Italian red wine. Amino Acids 36, 81–89 (2009). https://doi.org/10.1007/s00726-008-0035-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-008-0035-8