Abstract
In order to analyze the genes related to histamine production in halophilic lactic acid bacteria, 16 strains of histamine-producing bacteria were isolated from three fermented seafoods produced in the Hokuriku region of Japan. Phenotypic and 16S rRNA gene sequence analyses identified all of the strains as those of Tetragenococcus muriaticus. Pyruvoyl-dependent histidine decarboxylase gene (hdcA) was determined from all strains using the PCR method with an hdcA-specific detection primer set. Genetic analyses (Southern blot and restriction fragment length polymorphism analysis) of hdcA and genes related to histamine production (the hdc cluster) confirmed that all of the strains harbored 21–23 kbp plasmids encoding a single copy of hdcA. The four representative strains were selected based on isolation source and genetic analysis, and subsequently full sequences of plasmids harbored in these strains were determined. hdc cluster sequences from the plasmids showed very high similarity (>99 %) to known hdc clusters of T. halophilus, Lactobacillus hilgardii 0006, and other lactic acid bacteria. The structures of the plasmids, the replication region, the hdc cluster, and the plasmid maintenance system were conserved between the plasmids present in new isolates and the T. halophilus strains. These results indicate that plasmids encoding hdcA are widely distributed among T. halophilus and T. muriaticus and function in both species.
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References
Hungerford JM (2010) Scombroid poisoning: a review. Toxicon 56:231–243
Ladero V, Calles-Enriquez M, Fernández M, Alvarez MA (2010) Toxicological effects of dietary biogenic amines. Curr Nutr Food Sci 6:145–156
Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H, Grandvalet C, Coton E, Coton M, Barnavon L, Bach B, Rattray F, Bunte A, Magni C, Ladero V, Alvarez M, Fernández M, Lopez P, de Palencia PF, Corbi A, Trip H, Lolkema JS (2010) Biogenic amines in fermented foods. Eur J Clin Nutr 64:S95–S100
Hernandez-Herrero MM, Roig-Sages AX, Rodrigez-Jerez JJ, Mora-Ventura MT (1999) Halotolerant and halophilic histamine-forming bacteria isolated during the ripening of salted anchovies (Engraulis encrasicolus). J Food Prot 62:509–514
Landete JM, Ferrer S, Pardo I (2005) Which lactic acid bacteria are responsible for histamine production in wine? J Appl Microbiol 99:580–586
van Poelje PD, Snell EE (1990) Pyruvoyl-dependent enzyme. Annu Rev Biochem 59:29–59
Halász A, Baráth Á, Simon-Sarkadi L, Holzapfel W (1994) Biogenic amines and their production by microorganisms in food. Trends Food Sci Technol 5:42–49
Sato T, Fujii T, Masuda M, Okuzumi M (1994) Changes in numbers of histamine-metabolic bacteria and histamine content during storage of common mackerel. Fish Sci 60:299–302
Takahashi H, Kimura B, Yoshikawa M, Fujii T (2003) Cloning and sequencing of the histidine decarboxylase genes of Gram-negative, histamine-producing bacteria and their application in detection and identification of these organisms in fish. Appl Environ Microbiol 69:2568–2579
Yatsunami K, Echigo T (1991) Isolation of salt-tolerant histamine-forming bacteria from commercial rice-bran pickles of sardine. Nippon Suisan Gakkaishi 57:1723–1728 (in Japanese with English abstract)
Lonvaud-Funel A, Joyeux A (1994) Histamine production by wine lactic acid bacteria. Isolation of a histamine-producing strain of Leuconostoc oenos. J Appl Microbiol 77:401–407
Satomi M, Kimura B, Mizoi M, Sato T, Fujii T (1997) Tetragenococcus muriaticus sp. nov., a new moderately halophilic lactic acid bacterium isolated from fermented squid sauce. Int J Syst Bacteriol 47:832–836
Lonvaud-Funel A (2001) Biogenic amines in wines: role of lactic acid bacteria. FEMS Microbiol Lett 199:9–13
Lucas PM, Wolken WA, Claisse O, Lolkema JS, Lonvaud-Funel A (2005) Histamine-producing pathway encoded on an unstable plasmid in Lactobacillus hilgardii 0006. Appl Environ Microbiol 71:1417–1424
Martín MC, Fernández M, Linares DM, Alvarez MA (2005) Sequencing, characterization and transcriptional analysis of the histidine decarboxylase operon of Lactobacillus buchneri. Microbiology 151:1219–1228
Lucas PM, Claisse O, Lonvaud-Funel A (2008) High frequency of histamine-producing bacteria in the enological environment and instability of the histidine decarboxylase production phenotype. Appl Environ Microbiol 74:811–817
de las Rivas B, Rodríguez H, Carrascosa AV, Muñoz R (2008) Molecular cloning and functional characterization of a histidine decarboxylase from Staphylococcus capitis. J Appl Microbiol 104:194–203
Calles-Enríquez M, Eriksen BH, Andersen PS, Rattray FP, Johansen AH, Fernández M, Ladero V, Alvarez MA (2010) Sequencing and transcriptional analysis of the Streptococcus thermophilus histamine biosynthesis gene cluster: factors that affect differential hdcA expression. Appl Environ Microbiol 76:6231–6238
Tanase S, Guirard BM, Snell EE (1985) Purification and properties of a pyridoxal 5′-phosphate-dependent histidine decarboxylase from Morganella morganii AM-15. J Biol Chem 260:6738–6746
Huynh QK, Snell EE (1985) Pyruvoyl-dependent histidine decarboxylases. J Biol Chem 260:2798–2803
Vanderslice P, Copeland WC, Robertus JD (1986) Cloning and nucleotide sequence of wild type and a mutant histidine decarboxylase from Lactobacillus 30a. J Biol Chem 261:15186–15191
Joosten HMLJ, Northolt MD (1989) Detection, growth, and amine-producing capacity of lactobacilli in cheese. Appl Environ Microbiol 55:2356–2359
Coton E, Rollan GC, Lonvaud-Funel A (1998) Histidine carboxylase of Leuconostoc oenos 9204: purification, kinetic properties, cloning and nucleotide sequence of the hdc gene. J Appl Microbiol 84:143–151
Fujii T, Sakai H (1984) Chemical composition and microflora of fish sauce “Shottsuru”. Nippon Suisan Gakkaishi 50:1061–1066 (in Japanese with English abstract)
Ito H, Hadioetomo RS, Nikkuni S, Okada N (1985) Studies on lactic acid bacteria in fish sauces (part 1). Chemical composition and microflora of fish sauce. Rep Natl Food Res Inst 47:23–30
Ito H, Hadioetomo RS, Nikkuni S, Okada N (1985) Studies on lactic acid bacteria in fish sauces (part 2). Identification of salt-tolerance and acid-producing bacteria from fish sauce. Rep Natl Food Res Inst 47:31–40
Kobayashi K, Okuzumi M, Fujii T (1995) Microflora of fermented puffer fish ovaries in rice-bran “fugunoko nukazuke”. Fish Sci 61:291–295
Kuda T, Miyamoto H, Sakajiri M, Ando K, Yano T (2001) Microflora of fish nukazuke made in Ishikawa, Japan. Nippon Suisan Gakkaishi 67:296–301 (in Japanese with English abstract)
Kosaka Y, Kinoshita Y, Ooizumi T, Akahane Y (2010) Effects of temperature and NaCl content on production of taste-active components in heshiko during the aging process of salted mackerel with rice bran. Nippon Suisan Gakkaishi 76:392–398 (in Japanese with English abstract)
Funatsu Y, Sunago R, Konagaya S, Imai T, Kawasaki K, Takeshima F (2000) A comparison of extractive components of a fish sauce prepared from frigate mackerel using soy sauce koji with those of Japanese-made fish sauce and soy sauce. Nippon Suisan Gakkaishi 66:1036–1045
Taira W, Funatsu Y, Satomi M, Takano T, Abe H (2007) Changes in extractive components and microbial proliferation during fermentation of fish sauce from underutilized fish species and quality of final products. Fish Sci 73:913–923
Udomsil N, Rodtong S, Tanasupawat S, Yongsawatdigul J (2010) Proteinase-producing halophilic lactic acid bacteria isolated from fish sauce fermentation and their ability to produce volatile compounds. Int J Food Microbiol 141:186–194
Nakazato M, Kobayashi C, Yamajima Y, Tateishi Y, Kawai Y, Yasuda K (2002) Determination of volatile basic nitrogen (VBN) and non volatile amines in fish sauce. Annu Rep Tokyo Metrop Res Lab Public Health 53:95–100 (in Japanese with English abstract)
Fujii T, Kimura B, Mizoi M (2008) Changes in chemical composition and microbial flora during fermentation of squid sauce of Tobishima Island. Yamawaki Stud Arts Sci 46:121–131 (in Japanese with English abstract)
Kimura B, Konagaya Y, Fujii T (2001) Histamine formation by Tetragenococcus muriaticus, a halophilic lactic acid bacterium isolated from fish sauce. Int J Food Microbiol 70:71–77
Konagaya Y, Kimura B, Ishida M, Fujii T (2002) Purification and properties of a histidine decarboxylase from Tetragenococcus muriaticus, a halophilic lactic acid bacterium. J Appl Microbiol 92:1136–1142
Satomi M, Furushita M, Oikawa H, Yoshikawa-Takahashi M, Yano Y (2008) Analysis of a 30 kbp plasmid encoding histidine carboxylase gene in Tetragenococcus halophilus isolated from fish sauce. Int J Food Microbiol 126:202–209
Yokoi K, Harada Y, Shozen K, Satomi M, Taketo A, Kodaira K (2011) Characterization of the histidine decarboxylase gene of Staphylococcus epidermidis TYH1 coded on the staphylococcal cassette chromosome. Gene 477:32–41
Satomi M, Furushita M, Oikawa H, Yano Y (2011) Diversity of plasmid encoding histidine decarboxylase gene in Tetragenococcus spp. isolated from Japanese fish sauce. Int J Food Microbiol 148:60–65
Simu K, Holmfeldt K, Zweifel UL, Hagström Å (2005) Culturability and coexistence of colony-forming and single-cell marine bacterioplankton. Appl Environ Microbiol 71:4793–4800
Kosaka Y, Satomi M, Furutani A, Ooizumi T (2012) Microfloral and chemical changes during processing of heshiko produced by aging of salted mackerel with rice bran by means of conventional practice in Wakasa Bay area, Fukui, Japan. Fish Sci 78:485–490
Johnson JL (1981) Similarity analysis of DNAs. In: Gerhardt P et al (eds) Manual of methods for general bacteriology. American Society for Microbiology, Washington, DC, pp 658–659
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York
Garvie EL (1986) Genus Pediococcus Claussen 1903 68AL. In: Sneath PHA et al (eds) Bergey’s manual of systematic bacteriology, vol 2. The William and Wilkins Co., Baltimore, pp 1075–1079
Weiss N (1992) The genera Pediococcus and Aerococcus. In: Balows A et al (eds) The prokaryotes, vol 2, 2nd edn. Springer, New York, pp 1503–1507
Justé A, Lievens B, Frans I, Marsh TL, Klingeberg M, Michiels CW, Willems KA (2008) Genetic and physiological diversity of Tetragenococcus halophilus strains isolated from sugar- and salt-rich environments. Microbiology 154:2600–2610
Justé A, Van Trappen S, Verreth C, Cleenwerck I, De Vos P, Lievens B, Willems KA (2012) Characterization of Tetragenococcus strains from sugar thick juice reveals a novel species, Tetragenococcus osmophilus sp. nov., and divides Tetragenococcus halophilus into two subspecies, T. halophilus subsp. halophilus subsp. nov. and T. halophilus subsp. flandriensis subsp. nov. Int J Syst Evol Microbiol 62:129–137
Horii T, Nagasawa H, Nakayama J (2002) Functional analysis of TraA, the sex pheromone receptor encoded by pPD1, in a promoter region essential for the mating response in Enterococcus faecalis. J Bacteriol 184:6343–6350
Kurenbach B, Kopeć J, Mägdefrau M, Andreas K, Keller W, Bohn C, Abajy MY, Grohmann E (2006) The TraA relaxase autoregulates the putative type IV secretion-like system encoded by the broad-host-range Streptococcus agalactiae plasmid pIP501. Microbiology 152:637–645
Acknowledgments
The authors thank Dr. Y. Funatsu, T. Takano, and S. Shinya for supplying the samples. The technical assistance of N. Hatano and N. Sakai is gratefully acknowledged. Dr. J. Bruckner is acknowledged for helpful discussions. This research was partly supported by Research and Development Projects for Application in Promoting New Policy of Agriculture Forestry and Fisheries from the Ministry of Agriculture, Forestry and Fisheries, Japan.
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Satomi, M., Mori-Koyanagi, M., Shozen, Ki. et al. Analysis of plasmids encoding the histidine decarboxylase gene in Tetragenococcus muriaticus isolated from Japanese fermented seafoods. Fish Sci 78, 935–945 (2012). https://doi.org/10.1007/s12562-012-0512-6
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DOI: https://doi.org/10.1007/s12562-012-0512-6