Abstract
Histamine-producing bacteria were isolated from various types of canned salted anchovies with cooking oil, which were purchased from retail groceries over a study period of eight years. Thirty-two histamine-producing bacterial isolates were collected from 13 samples, which were equivalent to 43 % of the total canned anchovies manufactured in four different countries. All of these histamine-producing bacterial isolates were Gram-positive, catalase-negative, tetrad-forming cocci, and were identified as the lactic acid bacterium Tetragenococcus muriaticus by 16S rRNA gene sequence analysis. These findings indicated that histamine-producing T. muriaticus cells are widely distributed in the canned anchovies that were purchased from retail groceries. In addition, to evaluate the suppression of histamine production using a model of the storage condition of canned anchovies, the histamine-producing ability of our isolates under various culture conditions was examined. Low-pH and low-temperature conditions were demonstrated to be useful for inhibiting the histamine production of these isolates.
Similar content being viewed by others
References
Authority NF (2010) Presence of histamine in anchovies. NSW/FA/FI079/1007, 30. http://www.foodauthority.nsw.gov.au/_Documents/science/presence_of_histamine_in_anchovies.p. Accessed 03 October 2015
Cheftel H (1965) The processing of the anchovy: Engraulis encrasicholus linnaeus. In: Borgstrom G (ed) Fish as food. Academic Press, New York, pp 219–225
Collins MD, Facklam RR, Farrow JA, Williamson R (1989) Enterococcus raffinosus sp. nov., Enterococcus solitarius sp. nov. and Enterococcus pseudoavium sp. nov. FEMS Microbiol Lett 57:283–288
Ennahar S, Cai Y (2005) Biochemical and genetic evidence for the transfer of Enterococcus solitarius Collins et al. 1989 to the genus Tetragenococcus as Tetragenococcus solitarius comb. nov. Int J Syst Evol Microbiol 55:589–592
Feng C, Teuber S, Gershwin ME (2016) Histamine (scombroid) fish poisoning: a comprehensive review. Clinic Rev Allerg Immunol 50:64–69
Hungerford JM (2010) Scombroid poisoning: a review. Toxicon 56:231–243
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
Kim SH, Eun JB, Chen TY, Wei CI, Clemens RA, An H (2004) Evaluation of histamine and other biogenic amines and bacterial isolation in canned anchovies recalled by the USFDA. J Food Sci 69:M157–M162
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
Kobayashi T, Kimura B, Fujii T (2000a) Strictly anaerobic halophiles isolated from canned Swedish fermented herrings (Surströmming). Int J Food Microbiol 54:81–89
Kobayashi T, Kimura B, Fujii T (2000b) Differentiation of Tetragenococcus populations occurring in products and manufacturing processes of puffer fish ovaries fermented with rice-bran. Int J Food Microbiol 56:211–218
Kobayashi T, Kajiwara M, Wahyuni M, Kitakado T, Hamada-Sato N, Imada C, Watanabe E (2003) Isolation and characterization of halophilic lactic acid bacteria isolated from “terasi” shrimp paste: a traditional fermented seafood product in Indonesia. J Gen Appl Microbiol 49:279–286
Kobayashi T, Kajiwara M, Wahyuni M, Hamada‐Sato N, Imada C, Watanabe E (2004) Effect of culture conditions on lactic acid production of Tetragenococcus species. J Appl Microbiol 96:1215–1221
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
La Pietra L, Belfiore A, De Sio F, Voi AL, Pirone G (2014) Identification and characterization of halophilic bacteria from anchovy paste. Ind Conserve 2:15–35
Lee H, Kim SH, Sang CI, Jun H, Eun JB, An H (2005) Histamine and other biogenic amines and bacterial isolation in retail canned anchovies. J Food Sci 70:C145–C150
Moe NKT, Thwe SM, Shirai T, Terahara T, Imada C, Kobayashi T (2015) Characterization of lactic acid bacteria distributed in small fish fermented with boiled rice in Myanmar. Fish Sci 81:373–381
Mongkolthanaruk W, Nagase M, Kawai Y, Tanigawa K, Li Y, Yamaguchi T, Aimi T (2012) Evaluation of histamine productivity of Tetragenococcus halophilus isolated from salted mackerel (saba-shiokara). Fish Sci 78:441–449
Sato T, Horiuchi T, Nishimura I (2005) Simple and rapid determination of histamine in food using a new histamine dehydrogenase from Rhizobium sp. Anal Biochem 346:320–326
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 liver sauce. Int J Syst Bacteriol 47:832–836
Satomi M, Furushita M, Oikawa H, Yoshikawa-Takahashi M, Yano Y (2008) Analysis of a 30 kbp plasmid encoding histidine decarboxylase gene in Tetragenococcus halophilus isolated from fish sauce. Int J Food Microbiol 126:202–209
Satomi M, Furushita M, Oikawa H, Yano Y (2011) Diversity of plasmids encoding histidine decarboxylase gene in Tetragenococcus spp. isolated from Japanese fish sauce. Int J Food Microbiol 148:60–65
Satomi M, Mori-Koyanagi M, Shozen KI, Furushita M, Oikawa H, Yano Y (2012) Analysis of plasmids encoding the histidine decarboxylase gene in Tetragenococcus muriaticus isolated from Japanese fermented seafoods. Fish Sci 78:935–945
Sitdhipol J, Tanasupawat S, Tepkasikul P, Yukphan P, Tosukhowong A, Itoh T, Benjakul S, Visessanguan W (2013) Identification and histamine formation of Tetragenococcus isolated from Thai fermented food products. Ann Microbiol 63:745–753
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Thongsanit J, Tanasupawat S, Keeratipibul S, Jatikavanich S (2002) Characterization and identification of Tetragenococcus halophilus and Tetragenococcus muriaticus strains from fish sauce (Nam-pla). Jpn J Lactic Acid Bact 13:46–52
Villar M, de Ruiz Holgado AP, Sanchez JJ, Trucco RE, Oliver G (1985) Isolation and characterization of Pediococcus halophilus from salted anchovies (Engraulis anchoita). Appl Environ Microbiol 49:664–666
Acknowledgments
The authors are very grateful to Y. Komiyama and H. Tsuji in our laboratory for their technical assistance.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kobayashi, T., Wang, X., Shigeta, N. et al. Distribution of histamine-producing lactic acid bacteria in canned salted anchovies and their histamine production behavior. Ann Microbiol 66, 1277–1284 (2016). https://doi.org/10.1007/s13213-016-1213-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-016-1213-7