| BMC Microbiology | |
| Tyrosine-containing peptides are precursors of tyramine produced by Lactobacillus plantarum strain IR BL0076 isolated from wine | |
| Hervé Alexandre1  Stéphanie Weidmann1  Aurélie Rieu1  Cosette Grandvalet1  Maryse Bonnin-Jusserand1  | |
| [1] AgrosupDijon, Valmis UMR PAM, Université de Bourgogne, Institut Universitaire de la Vigne et du Vin Jules Guyot, rue Claude Ladrey, BP 27877, 21078, Dijon Cedex, France | |
| 关键词: Wine; Lactobacillus plantarum; Peptides; Tyramine; | |
| Others : 1221765 DOI : 10.1186/1471-2180-12-199 |
|
| received in 2012-03-20, accepted in 2012-08-31, 发布年份 2012 | |
PDF
|
|
【 摘 要 】
Background
Biogenic amines are molecules with allergenic properties. They are found in fermented products and are synthesized by lactic acid bacteria through the decarboxylation of amino acids present in the food matrix. The concentration of biogenic amines in fermented foodstuffs is influenced by many environmental factors, and in particular, biogenic amine accumulation depends on the quantity of available precursors. Enological practices which lead to an enrichment in nitrogen compounds therefore favor biogenic amine production in wine. Free amino acids are the only known precursors for the synthesis of biogenic amines, and no direct link has previously been demonstrated between the use of peptides by lactic acid bacteria and biogenic amine synthesis.
Results
Here we demonstrate for the first time that a Lactobacillus plantarum strain isolated from a red wine can produce the biogenic amine tyramine from peptides containing tyrosine. In our conditions, most of the tyramine was produced during the late exponential growth phase, coinciding with the expression of the tyrDC and tyrP genes. The DNA sequences of tyrDC and tyrP in this strain share 98% identity with those in Lactobacillus brevis consistent with horizontal gene transfer from L. brevis to L. plantarum.
Conclusion
Peptides amino acids are precursors of biogenic amines for Lactobacillus plantarum strain IR BL0076.
【 授权许可】
2012 Bonnin-Jusserand et al.; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
|---|---|---|---|
| 20150803133905785.pdf | 638KB | ||
| Figure 4. | 22KB | Image | |
| Figure 3. | 33KB | Image | |
| Figure 2. | 32KB | Image | |
| Figure 1. | 35KB | Image |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
【 参考文献 】
- [1]Silla Santos MH: Biogenic amines: their importance in foods. Int J Food Microbiol 1996, 29:213-231.
- [2]Bauza T, Blaise A, Teissedre PL, Cabanis JC, Kanny G, Moneret-Vautrin DA, Daumas F: Les amines biogènes du vin: metabolisme et toxicité. Bulletin de l’OIV 1995, 68:42-67.
- [3]Hannington E: Preliminary report on tyramine headache. Br Med J 1967, 2:550-551.
- [4]Marques AP, Leitao MC, San Romao MV: Biogenic amines in wines: influence of oenological factors. Food Chem 2008, 107:853-860.
- [5]Konings WN, Lolkema JS, Bolhuis H, Van Veen HW, Poolman B, Driessen AJM: The role of transport processes in survival of lactic acid bacteria. Antonie Leeuwenhoek 1997, 71:117-128.
- [6]Molenaar D, Bosscher JS, Brink BT, Driessen AJM, Konings WN: Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in lactobacillus buchneri. J Bacteriol 1993, 175:2864-2870.
- [7]Wolken WAM, Lucas PM, Lonvaud-Funel A, Lolkema JS: The mechanism of the tyrosine transporter TyrP supports a proton motive tyrosine decarboxylation pathway in lactobacillus brevis. J Bacteriol 2006, 188:2198-2206.
- [8]Lonvaud-Funel A, Joyeux A: Histamine production by wine lactic acid bacteria: isolation of a histamine-producing strain of leuconostoc oenos. J Appl Microbiol 1994, 77:401-407.
- [9]Marcobal AB, De Las Rivas B, Moreno-Arribas MV, Munoz R: Identification of the ornithine decarboxylase gene in the putrescine-producer oenococcus oeni BIFI-83. FEMS Microbiol Lett 2004, 239:213-220.
- [10]Moreno-Arribas V, Torlois S, Joyeux A, Bertrand A, Lonvaud-funel A: Isolation, properties and behaviour of tyramine-producing lactic acid bacteria from wine. J Appl Microbiol 2000, 88:584-593.
- [11]Guerrini S, Mangani S, Granchi L, Vincenzini M: Biogenic amine production by oenococcus oeni. Curr Microbiol 2002, 44:374-378.
- [12]Coton E, Coton M: Evidence of horizontal transfer as origin of strain to strain variation of the tyramine production trait in lactobacillus brevis. Food Microbiol 2009, 26:52-57.
- [13]Connil N, Le Breton Y, Dousset X, Auffray Y, Rincé A, Prévost H: Identification of the enterococcus faecalis tyrosine decarboxylase operon involved in tyramine production. Appl Environ Microbiol 2002, 68:3537-3544.
- [14]Fernández M, Linares DM, Alvarez MA: Sequencing of the tyrosine decarboxylase cluster of lactococcus lactis IPLA 655 and the development of a PCR method for detecting tyrosine decarboxylating lactic acid bacteria. J Food Prot 2004, 67:2521-2529.
- [15]Lucas P, Landete J, Coton M, Coton E, Lonvaud-Funel A: The tyrosine decarboxylase operon of lactobacillus brevis IOEB 9809: characterization and conservation in tyramine-producing bacteria. FEMS Microbiol Lett 2003, 229:65-71.
- [16]Gardini F, Zaccarelli A, Belletti N, Faustini F, Cavazza A, Martuscelli M, Mastrocola D, Suzzi G: Factors influencing biogenic amine production by a strain of oenoccocus oeni in a model system. Food Control 2005, 16:609-616.
- [17]Hernandez-Orte P, Pena-Gallego A, Ibarz MJ, Cacho J, Ferreira V: Determination of the biogenic amines in musts and wines before and after malolactic fermentation using 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate as the derivatizing agent. J Chrom A 2006, 1129:160-164.
- [18]Herbert P, Cabrita MJ, Ratola N, Laureano O, Alves A: Free amino acids and biogenic amines in wines and musts from the Alentejo region. Evolution of amines during alcoholic fermentation and relationship with variety, sub-region and vintage. J Food Eng 2005, 66:315-322.
- [19]Lonvaud-Funel A: Biogenic amines in wines: role of lactic acid bacteria. FEMS Microbiol Lett 2001, 199:9-13.
- [20]Solieri L, Genova F, De Paola M, Giudici P: Characterization and technological properties of oenococcus oeni strains from wine spontaneous malolactic fermentations: a framework for selection of new starter cultures. J Appl Microbiol 2010, 108:285-298.
- [21]Pessione E, Mazzoli R, Giuffrida MG, Lamberti C, Garcia-Moruno E, Barello C, Conti A, Giunta C: A proteomic approach to studying biogenic amine producing lactic acid bacteria. Proteomics 2005, 5:687-689.
- [22]Soufleros EH, Bouloumpasi E, Zotou A, Loukou Z: 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 2007, 101:704-716.
- [23]Pereira V, Pontes M, Camara JS, Marques JC: Simultaneous analysis of free amino acids and biogenic amines in honey and wine samples using in loop orthophthalaldeyde derivatization procedure. J Chrom A 2008, 1189:435-443.
- [24]Bach B, Colas S, Massini L, Barnavon L, Vuchot P: Effect of nitrogen addition during alcoholic fermentation on the final content of biogenic amines in wine. Ann Microbiol 2010, 61:185-190.
- [25]Babayan TL, Bezrukov MG: Autolysis in yeasts. Acta Biotechnol 1985, 2:129-136.
- [26]Alexandre H, Heintz D, Chassagne D, Guilloux-Benatier M, Charpentier C, Feuillat M: Protease A activity and nitrogen fractions released during alcoholic fermentation and autolysis in enological conditions. J Ind Microbiol Biot 2001, 26:235-240.
- [27]Bozdogan A, Canbas A: Influence of yeast strain, immobilisation and ageing time on the changes of free amino acids and amino acids in peptides in bottle-fermented sparkling wines obtained from vitis vinifera cv. Emir. Int J of Food Sci Tech 2011, 46:1113-1121.
- [28]Feuillat M, Brillant G, Rochard J: Mise en évidence d’une production de proteases exocellulaires par les levures au cours de la fermentation alcoolique du moût de raisin. Connais Vigne Vin 1980, 14:37-52.
- [29]de Nadra MC M, Farias ME, Moreno-Arribas MV, Pueyo E, Polo MC: Proteolytic activity of leuconostoc oenos. Effect on proteins and polypeptides from white wine. FEMS Microbiol Lett 1997, 150:135-139.
- [30]de Manca Nadra MC, Farias ME, Moreno-Arribas MV, Pueyo E, Polo MC: A proteolytic effect of oenococcus oeni on the nitrogenous macromolecular fraction of red wine. FEMS Microbiol Lett 1999, 174:41-47.
- [31]Folio P, Ritt JF, Alexandre H, Remize F: Characterization of EprA, a major extracellular protein of oenococcus oeni with protease activity. Int J Food Microbiol 2008, 127:26-31.
- [32]Leitao MC, Teixeira HC, Barreto Crespo MT, San Romao MV: Biogenic amines occurrence in wine. Amino acid decarboxylase and proteolytic activities expression by oenococcus oeni. J Agric Food Chem 2000, 48:2780-2784.
- [33]Strahinic I, Kojic M, Tolinacki M, Fira D, Topisirovic L: The presence of prtP proteinase gene in natural isolate lactobacillus plantarum BGSJ3-18. Lett Appl Microbiol 2009, 50:43-49.
- [34]Kunji ERS, Smid EJ, Plapp R, Poolman B, Konings WN: Di-tripeptides and oligopeptides are taken up via distinct transport mechanisms in lactococcus lactis. J Bacteriol 1993, 175:2052-2059.
- [35]Fang G, Konings WN, Poolman B: Kinetics and substrate specificity of membrane-reconstituted peptide transporter DtpT of lactococcus lactis. J Bacteriol 2000, 182:2530-2535.
- [36]Sanz Y, Toldra F, Renault P, Poolman B: Specificity of the second binding protein of the peptide ABC-transporter (Dpp) of lactococcus lactis IL1403. FEMS Microbiol Lett 2003, 227:33-38.
- [37]Kleerebezem M, Boekhorst J, Van Kranenburg R, Molenaar D, Kuipers OP, Leer R, Tarchini R, Peters SA, Sandbrink HM, Fiers MWEJ, Stiekema W, Klein Lankhorst RM, Bron PA, Hoffer SM, Nierop Groot MN, Kerkhoven R, De Vries M, Ursing B, De Vos WM, Siezen RJ: Complete genome sequence of lactobacillus plantarum WCFS1. PNAS 2003, 100:1990-1995.
- [38]Varmanen P, Vesanto E, Steele JL, Palva A: Characterization and expression of the PepN gene encoding a general aminopeptidase from lactobacillus helveticus. FEMS Microbiol Lett 1994, 124:315-320.
- [39]Tsakalidou E, Dalezios I, Georgalaki M, Kalantzopoulos G: A comparative study: aminopeptidase activities from lactobacillus delbrueckii ssp. bulgaricus and streptococcus thermophilus. J Dairy Sci 1993, 76:2145-2151.
- [40]Tan PST, Van Alen-Boerrigter IT, Poolman B, Siezen RJ, De Vos WM, Konings WN: Characterization of the lactococcus lactis pepN gene encoding an aminopeptidase homologous to mammalian aminopeptidase N. FEBS 1992, 306:9-16.
- [41]Hwang IK, Kaminogawa S, Yamauchi K: Purification and properties of a dipeptidase from streptococcus cremoris. Agric Biol Chem 1981, 45:159-166.
- [42]Arena ME, Fiocco D, de Manca Nadra MC, Pardo I, Spano G: Characterization of a lactobacillus plantarum strain able to produce tyramine and partial cloning of a putative tyrosine decarboxylase gene. Curr Microbiol 2007, 55:205-210.
- [43]Torriani S, Felis GE, Dellaglio F: Differentiation of lactobacillus plantarum, L. pentosus, and L. paraplantarum by recA gene sequence analysis and multiplex PCR assay with recA gene-derived primers. Appl Environ Microbiol 2001, 67:3450-3454.
- [44]Teusink B, Van Enckevort FHJ, Francke C, Wiersma A, Wegkamp A, Smid EJ, Siezen RJ: In silico reconstruction of the metabolic pathways of lactobacillus plantarum: comparing predictions of nutrient requirements with those from growth experiments. Appl Environ Microbiol 2005, 71:7253-7262.
- [45]Pereira CI, Barreto Crespo MT, San Romao MV: Evidence for proteolytic activity and biogenic amines production in lactobacillus curvatus and L. homohiochii. Int J Food Microbiol 2001, 68:211-216.
- [46]Kunji ERS, Mierau I, Hagting A, Poolman B, Konings WN: The proteolytic system of lactic acid bacteria. Antonie Leeuwenhoek 1996, 70:187-221.
- [47]Gomez-Alonso S, Hermosian-Gutearrez I, Garcia-Romero E: Simultaneous HPLC analysis of biogenic amines, amino acids, and ammonium ion as aminoenone derivatives in wine and beer samples. J Agric Food Chem 2007, 55:608-613.
- [48]Leitao MC, Marques AP, San Romao MV: A survey of biogenic amines in commercial Portuguese wines. Food Control 2005, 16:199-204.
- [49]Coton M, Fernandez M, Trip H, Ladero V, Mulder NL, Lolkema JS, Alvarez MA, Coton E: Characterization of the tyramine-producing pathway in sporolactobacillus sp P3J. Microbiology 2011, 157:1841-1849.
- [50]Calles-Enriquez M, Hjort Eriksen B, Skov Andersen P, Rattray FP, Johansen AH, Fernandez M, Ladero V, Alvarez MA: Sequencing and transcriptional analysis of the streptococcus thermophilus histamine biosynthesis gene cluster: factors that affect differential hdcA expression. Appl Environ Microbiol 2010, 76:6231-6238.
- [51]Bely M, Sablayrolles JM, Barre P: Automatic detection of assimilable nitrogen deficiencies during alcoholic fermentation in oenological conditions. J Ferment Bioeng 1991, 70:246-252.
- [52]Gonzales Marco A, Moreno NJ, Ancin Azpilicueta C: Influence of addition of yeast autolysate on the formation of amines in wine. J Sci Food Agric 2006, 86:2221-2227.
- [53]Terrade N, Noel R, Couillaud R, De Mira Orduna R: A new chemically defined medium for wine lactic acid bacteria. Food Res Int 2009, 42:363-367.
- [54]Wilmotte A, Van der Auwera G, De Wachter R: Structure of the 16S ribosomal RNA of the thermophilic cynobacterium chlorogloeopsis HTF (dMastigocladus laminosus HTFT) strain PCC7518, and phylogenetic analysis. FEBS Lett 1993, 317:96-100.
- [55]Nannelli F, Claisse O, Gindreau E, De Revel G, Lonvaud-Funel A, Lucas PM: Determination of lactic acid bacteria producing biogenic amines in wine by quantitative PCR methods. Lett Appl Microbiol 2008, 47:594-599.
- [56]Duary RK, Batish VK, Grover S: Expression of the atpD gene in probiotic lactobacillus plantarum strains under in vitro acidic conditions using RT-qPCR. Res Microbiol 2010, 161:399-405.
- [57]Fiocco D, Crisetti E, Capozzi V, Spano G: Validation of an internal control gene to apply reverse transcription quantitative PCR to study heat, cold and ethanol stresses in lactobacillus plantarum. World J Microbiol Biotechnol 2008, 24:899-902.
PDF