The capability of tyramine production and correlation between phenotypic and genetic characteristics of Enterococcus faecium and Enterococcus faecalis strains

Frontiers in Microbiology

Volumn 6, Issue DEC, 2015, Pages

  Bargossi, Eleonora ^a   Gardini, Fausto ^a   Gatto, Veronica ^b   Montanari, Chiara ^a   Torriani, Sandra ^b   Tabanelli, Giulia ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

Author keywords

Enterococcus faecalis; Enterococcus faecium; Gene expression; Tyramine; Tyrosine decarboxylase activity

Indexed keywords

SODIUM PROTON EXCHANGE PROTEIN; TYRAMINE; TYROSINE DECARBOXYLASE;

ARTICLE; BACTERIAL STRAIN; CELL VIABILITY; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENZYME ACTIVITY; ENZYME PURIFICATION; GENE SEQUENCE; GENETIC ORGANIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHENOTYPE; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TEMPERATURE;

EID: 84954192615     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01371     Document Type: Article

References (46)

1. Bargossi, E., Tabanelli, G., Montanari, C., Lanciotti, R., Gatto, V., Gardini, F., et al. (2015). Tyrosine decarboxylase activity of enterococci grown in media with different nutritional potential: tyramine and 2-phenylethylamine accumulation and tyrDC gene expression. Front. Microbiol. 6:259. doi: 10.3389/fmicb.2015.00259
2. Beshkova, D., and Frengova, G. (2012). Bacteriocins from lactic acid bacteria: microorganisms of potential biotechnological importance for the dairy industry. Eng. Life Sci. 12, 419-432. doi: 10.1002/elsc.201100127
3. Bunková, L., Bunka, F., Pollaková, E., Podešvová, T., and Dráb, V. (2011). The effect of lactose, NaCl and an aero/anaerobic environment on the tyrosine decarboxylase activity of Lactococcus lactis subsp. cremoris and Lactococcus lactis subsp. lactis. Int. J. Food Microbiol. 147, 112-119. doi: 10.1016/j.ijfoodmicro.2011.03.017
4. Connil, N., Le Breton, Y., Dousset, X., Auffray, Y., Rincé, A., and Prévost, H. (2002). Identification of the Enterococcus faecalis tyrosine decarboxylase operon involved in tyramine production. Appl. Environ. Microbiol. 68, 3537-3544. doi: 10.1128/AEM.68.7.3537-3544.1002
5. EFSA (2011). Scientific opinion on risk based control of biogenic amine formation in fermented foods. EFSA J. 9, 2393-2486.
6. Fernández, M., Linares, D. M., Rodríguez, A., and Alvarez, M. A. (2007). Factors affecting tyramine production in Enterococcus durans IPLA 655. Appl. Microbiol. Biotechnol. 73, 1400-1406. doi: 10.1007/s00253-006-0596-y
7. Fernández, M., and Zúñiga, M. (2006). Amino acid catabolic pathways of lactic acid bacteria. Crit. Rev. Microbiol. 32, 155-183. doi: 10.1080/10408410600880643
8. Fontana, C., Cocconcelli, P. S., Vignolo, G., and Saavedra, L. (2015). Occurrence of antilisterial structural bacteriocins genes in meat borne lactic acid bacteria. Food Control 47, 53-59. doi: 10.1016/j.foodcont.2014.06.021
9. Foulquié Moreno, M. R., Sarantinopoulos, P., Tsakalidou, E., and De Vuyst, L. (2006). The role and application of enterococci in food and health. Int. J. Food. Microbiol. 106, 1-24. doi: 10.1016/j.ijfoodmicro.2005.06.026
10. Franz, C. M. A. P., Holzapfel, W. H., and Stiles, M. E. (1999). Enterococci at the crossroads of food safety? Int. J. Food Microbiol. 47, 1-24. doi: 10.1016/S0168-1605(99)00007-0
11. Franz, C. M. A. P., Huch, M., Abriouel, H., Holzapfel, W., and Gálvez, A. (2011). Enterococci as probiotics and their implications in food safety. Int. J. Food Microbiol. 151, 125-140. doi: 10.1016/j.ijfoodmicro.2011.08.014
12. Gardini, F., Bover-Cid, S., Tofalo, R., Belletti, N., Gatto, V., Suzzi, G., et al. (2008). Modeling the aminogenic potential of Enterococcus faecalis EF37 in dry fermented sausages through chemical and molecular approaches. Appl. Environ. Microbiol. 74, 2740-2750. doi: 10.1128/AEM.02267-07
13. Gardini, F., Martuscelli, M., Caruso, M. C., Galgano, F., Crudele, M. A., Favati, F., et al. (2001). Effects of pH, temperature and NaCl concentration on the growth kinetics, proteolytic activity and biogenic amine production of Enterococcus faecalis. Int. J. Food Microbiol. 64, 105-117. doi: 10.1016/S0168-1605(00)00445-1
14. Gautheret, D., and Lambert, A. (2001). Direct RNA motif definition and identification from multiple sequence alignments using secondary structure profiles. J. Mol. Biol. 313, 1003-1011. doi: 10.1006/jmbi.2001.5102
15. Giraffa, G. (2002). Enterococci from foods. FEMS Microbiol. Rev. 26, 163-171. doi: 10.1111/j.1574-6976.2002.tb00608.x
16. Giraffa, G. (2003). Functionality of enterococci in dairy products. Int. J. Food Microbiol. 88, 215-222. doi: 10.1016/S0168-1605(03)00183-1
17. Hollenbeck, B. L., and Rice, L. B. (2012). Intrinsic and acquired resistance mechanisms in enterococcus. Virulence 3, 421-569. doi: 10.4161/viru.21282
18. Klein, G. (2003). Taxonomy, ecology and antibiotic resistance of enterococci from food and the gastro-intestinal tract. Int. J. Food Microbiol. 88, 123-131. doi: 10.1016/S0168-1605(03)00175-2
19. Komprda, T., Burdychová, R., Dohnal, V., Cwiková, O., and Sládková, P. (2008). Some factors influencing biogenic amines and polyamines content in Dutch-type semi-hard cheese. Eur. Food Res. Technol. 227, 29-36. doi: 10.1007/s00217-007-0688-7
20. Ladero, V., Fernández, M., Calles-Enríquez, M., Sánchez Llana, E., Cañedo, E., Martin, M. C., et al. (2012). Is the production of the biogenic amines tyramine and putrescine a species-level trait in enterococci? Food Microbiol. 30, 132-138. doi: 10.1016/j.fm.2011.12.016
21. Ladero, V., Linares, D. M., del Rio, B., Fernandez, M., Martin, M. C., and Alvarez, M. A. (2013). Draft genome sequence of the tyramine producer Enterococcus durans strain IPLA 655. Genome Announc. 3:e265. doi: 10.1128/genomeA.00265-13
22. Leuschner, R. G. K., Kurihara, R., and Hammes, W. P. (1999). Formation of biogenic amines by proteolytic enterococci during ripening. J. Sci. Food Agric. 79, 1141-1144. doi: 10.1002/(SICI)1097-0010(199906)79:83.0.CO;2-0
23. Linares, D. M., Fernández, M., Martín, M. C., and Alvarez, M. A. (2009). Tyramine biosynthesis in Enterococcus durans is trascriptionally regulated by the extracellular pH and tyrosine concentration. Microbiol. Biotechnol. 2, 625-633. doi: 10.1111/j.1751-7915.2009.00117.x
24. Linares, D. M., Martín, M. C., Ladero, V., Alvarez, M. A., and Fernández, M. (2011). Biogenic amines in dairy products. Crit. Rev. Food Sci. Nutr. 51, 691-703. doi: 10.1080/10408398.2011.582813
25. Liu, F., Xu, W., Du, L., Wang, D., Zhu, Y., Geng, Z., et al. (2014). Heterologous expression and characterization of tyrosine decarboxylase from Enterococcus faecalis R612Z1 and Enterococcus faecium R615Z1. J. Food Protect. 77, 592-598. doi: 10.4315/0362-028X.JFP-13-326
26. Macke, T. J., Ecker, D. J., Gautheret, D., Case, D. A., and Sampath, R. (2001). RNAMotif, an RNA secondary structure definition and search algorithm. Nucleic Acids Res. 29, 4724-4735. doi: 10.1093/nar/29.22.4724
27. Marcobal, A., De Las Rivas, B., Landete, J. M., Tabera, L., and Muñoz, R. (2012). Tyramine and phenylethylamine biosynthesis by food bacteria. Crit. Rev. Food Sci. Nutr. 52, 448-467. doi: 10.1080/10408398.2010.500545
28. Marcobal, A., de las Rivas, B., and Muñoz, R. (2006). First genetic characterization of a bacterial β-phenylethylamine biosynthetic enzyme in Enterococcus faecium RM58. FEMS Microbiol. Lett. 258, 144-149. doi: 10.1111/j.1574-6968.2006.00206.x
29. Masson, F., Talon, R., and Montel, M. C. (1996). Histamine and tyramine production by bacteria from meat products. Int. J. Food Microbiol. 32, 199-207. doi: 10.1016/0168-1605(96)01104-X
30. McCabe-Sellers, B., Staggs, C. G., and Bogle, M. L. (2006). Tyramine in foods and monoamine oxidase inhibitor drugs: a crossroad where medicine, nutrition, pharmacy, and food industry converge. J. Food Comp. Anal. 19, S58-S65. doi: 10.1016/j.jfca.2005.12.008
31. McWilliam, H., Li, W., Uludag, M., Squizzato, S., Park, Y. M., Buso, N., et al. (2013). Analysis tool web services from the EMBL-EBI. Nucleic Acids Res. 41, W597-W600. doi: 10.1093/nar/gkt376
32. Minogue, T. D., Daligault, H. E., Davenport, K. W., Broomall, S. M., Bruce, D. C., Chain, P. S., et al. (2014). Complete genome assembly of Enterococcus faecalis 29212, a laboratory reference strain. Genome Announc. 2, pii:e00968-e01014. doi: 10.1128/genomeA.00968-14
33. Molenaar, D., Bosscher, J. S., ten Brink, B., Driessen, A. J., and Konings, W. N. (1993). Generation of a proton motive force by histidine decarboxylation and electrogenic histidine/histamine antiport in Lactobacillus buchneri. J. Bacteriol. 175, 2864-2870.
34. Moreno-Arribas, V., and 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. doi: 10.1111/j.1574-6968.1999.tb08777.x
35. Moreno-Arribas, V., and Lonvaud-Funel, A. (2001). Purification and characterization of tyrosine decarboxylase of Lactobacillus brevis IOEB 9809 isolated from wine. FEMS Microbiol. Lett. 195, 103-107. doi: 10.1111/j.1574-6968.2001.tb10505.x
36. Pereira, C. I., Matos, D., San Romaõ, M. V., and Barreto Crespo, M. T. (2009). Dual role for the tyrosine decarboxylation pathway in Enterococcus faecium E17: response to an acid challenge. Appl. Environ. Microbiol. 75, 345-352. doi: 10.1128/AEM.01958-08
37. Perez, M., Calles-Enríquez, M., Nes, I., Martin, M. C., Fernandez, M., Ladero, V., et al. (2015). Tyramine biosynthesis is transcriptionally induced at low pH and improves the fitness of Enterococcus faecalis in acidic environments. Appl. Microbiol. Biotechnol. 99, 3547-3558. doi: 10.1007/s00253-014-6301-7
38. Pérez-Martín, F., Seseña, S., Miguel Izquierdo, P., and Palop, M. L. (2014). Are Enterococcus populations present during malolactic fermentation of red wine safe? Food Microbiol. 42, 95-101. doi: 10.1016/j.fm.2014.03.001
39. Pessione, E., Pessione, A., Lamberti, C., Coïsson, D. J., Riedel, K., Mazzoli, R., et al. (2009). First evidence of a membrane-bound, tyramine and β-phenylethylamine producing, tyrosine decarboxylase in Enterococcus faecalis: a two-dimensional electrophoresis proteomic study. Proteomics 9, 2695-2710. doi: 10.1002/pmic.200800780
40. Rossi, F., Rizzotti, L., Felis, G. E., and Torriani, S. (2014). Horizontal gene transfer among microorganisms in food: current knowledge and future perspectives. Food Microbiol. 42, 232-243. doi: 10.1016/j.fm.2014.04.004
41. Sandmeier, E. (1994). Multiple evolutionary origin of pyridoxal-5'-phosphate-dependent amino acid decarboxylases. Eur. J. Biochem. 221, 997-1002. doi: 10.1111/j.1432-1033.1994.tb18816.x
42. Shalaby, A. R. (1994). Significance of biogenic amines to food safety and human health. Food Res. Int. 29, 675-690. doi: 10.1016/S0963-9969(96)00066-X
43. Solovyev, V., and Salamov, A. (2011). "Automatic annotation of microbial genomes and metagenomic sequences" in Metagenomics and its Applications in Agriculture, Biomedicine and Environmental Studies, ed. R. W. Li (Hauppauge, NY: Nova Science Publishers), 61-78.
44. Suzzi, G., and Gardini, F. (2003). Biogenic amines in dry fermented sausages: a review. Int. J. Food Microbiol. 88, 41-54. doi: 10.116/S0168-1605(03)00080-1
45. Tabanelli, G., Torriani, S., Rossi, F., Rizzotti, L., and Gardini, F. (2012). Effect of chemico-physical parameters on the histidine decarboxylase (HdcA) enzymatic activity in Streptococcus thermophilus PRI60. J. Food Sci. 77, M231-M237. doi: 10.1111/j.1750-3841.2012.02628.x
46. Wolken, W. A. M., Lucas, P., Lonvaud-Funel, A., and Lolkema, J. (2006). The mechanism of the tyrosine transporter TyrP supports a proton motive tyrosine decarboxylation pathway in Lactobacillus brevis. J. Bacteriol. 188, 2198-2206. doi: 10.1128/JB.188.6.2198-2206.2006