Bacterial community associated to histamine contamination in sardines: a case study in the canned fish industry
DOI:
https://doi.org/10.20950/1678-2305/bip.2024.50.e886Keywords:
Histamine, Canned Fish, Scombrotoxin, Fish Poisoning, Fishing IndustryAbstract
This study aimed to identify the predominant bacterial populations in sardine samples with high histamine content (≥ 200 mg*kg-1) and histamine-free (< 1 mg*kg-1). For this study, 1,000 g of muscle samples were collected from 40–45 sardines per batch, all obtained from the same supplier, fishing area and period, for histamine analysis. Samples (1 g) from five different batches with ≥ 200 mg*kg-1 of histamine (named histamine group) and five with < 1 mg*kg-1 (named no-histamine group) were submitted to microbial analysis by extracting the total DNA, followed by polymerase chain reaction of the V3-V4 region of 16S rRNA gene and Ilumina sequencing (Mi-Seq, paired-end). In total, 18 different operational taxonomic units were identified in all samples. Sardines with high histamine content exhibited lower microbial diversity and a higher abundance of the genera Photobacterium and Shewanella. These bacteria thrive under mild temperatures and indicate fish spoilage and the production of biogenic amines. In contrast, Psychrobacter and Pseudoalteromonas, known to withstand harsh conditions, including low temperatures, were more prevalent in histamine-free sardines. Our findings point out to a marked change in the bacterial community of sardines with high and no histamine content, even though they are from the same fishing area, period, and shipment.
References
Ayala-del-Río, H. L., Chain, P. S., Grzymski, J. J., Ponder, M. A., Ivanova, N., Bergholz, P. W., Di Bartoli, G., Hauser, L. L. M., & Bakermans, C. (2010). The genome sequence of Psychrobacter arcticus 273-4, a psychroactive Siberian permafrost bacterium, reveals mechanisms for adaptation to low-temperature growth. Applied and Environmental Microbiology, 76(7), 2304-2312. https://doi.org/10.1128/AEM.02101-09
Bita, S., & Sharifian, S. (2024). Assessment of biogenic amines in commercial tuna fish: Influence of species, capture method, and processing on quality and safety. Food Chemistry, 435, 137576. https://doi.org/10.1016/j.foodchem.2023.137576
Bjornsdottir-Butler, K., May, S., Hayes, M., Abraham, A., & Benner Jr., R. A. (2020). Characterization of a novel enzyme from Photobacterium phosphoreum with histidine decarboxylase activity. International Journal of Food Microbiology, 334, 108815. https://doi.org/10.1016/j.ijfoodmicro.2020.108815
Bowman, J. P., McCammon, S. A., Brown, M. V., Nichols, D. S., & McMeekin, T. A. (1997). Diversity and association of psychrophilic bacteria in Antarctic sea ice. Applied and Environmental Microbiology, 63(8), 3068-3078. https://doi.org/10.1128/aem.63.8.3068-3078.1997
Bozal, N., Montes, M. J., Tudela, E., & Guinea, J. (2003). Characterization of several Psychrobacter strains isolated from Antarctic environments and description of Psychrobacter luti and Psychrobacter fozii. International Journal of Systematic and Evolutionary Microbiology, 53(4), 1093-1100. https://doi.org/10.1099/ijs.0.02457-0
Burtseva, O., Kublanovskaya, A., Baulina, O., Fedorenko, T., Lobakova, E., & Chekanov, K. (2020). The strains of bioluminescent bacteria isolated from the White Sea finfishes: Genera Photobacterium, Aliivibrio, Vibrio, Shewanella, and first luminous Kosakonia. Journal of Photochemistry and Photobiology B: Biology, 208, 111895. https://doi.org/10.1016/j.jphotobiol.2020.111895
Cicero, A., Cammilleri, G., Galluzzo, F. G., Calabrese, I., Pulvirenti, A., Giangrosso, G., Cicero, N., Cumbo, V., Vella, A., Macaluso, A., & Ferrantelli, V. (2020). Histamine in fish products randomly collected in Southern Italy: a 6-year study. Journal of Food Protection, 83(2), 241-248. https://doi.org/10.4315/0362-028X.JFP-19-305
Christoff et al. (2017). White paper Neoporspeta: Bacterial identification through accurate library preparation and high-throughput sequencing. Retrieved from https://www.neoprospecta.com/conteudo/whitepaper-microbioma-e-iras/
Deng, H., Wu, G., Zhou, L., Chen, X., Guo, L., Luo, S., & Yin, Q. (2024). Microbial contribution to 14 biogenic amines accumulation in refrigerated raw and deep-fried hairtails (Trichiurus lepturus). Food Chemistry, 443, 138509. https://doi.org/10.1016/j.foodchem.2024.138509
Ding, T., & Li, Y. (2024). Biogenic amines are important indices for characterizing the freshness and hygienic quality of aquatic products: A review. LWT - Food Science and Technology, 194, 115793. https://doi.org/10.1016/j.lwt.2024.115793
Farmer, J. J., & Janda, M. J. (2015). Vibrionaceae. In: W. B. Whitman (ed.), Bergey’s Manual of Systematic of Archeae and Bacteria (pp. 491-494). Wiley-Blackwell.
Food and Agriculture Organization of the United Nations (FAO) (2022). The state of world fisheries and aquaculture: Towards blue transformation. FAO. https://doi.org/10.4060/cc0461en
Food and Drug Administration (FDA) (2020). Scombrotoxin (histamine) formation. In B. Leonard (Ed.), Fish and fishery products hazards and controls guidance (pp. 83-102). FDA.
González, C. J., Santos, J. A., García-López, M. L., & Otero, A. (2000). Psychrobacters and related bacteria in freshwater fish. Journal of Food Protection, 63(3), 315-321. https://doi.org/10.4315/0362-028X-63.3.315
Gram, L. (2009). Microbiological spoilage of fish and seafood products. In W. Sperber & M. Doyle (Eds.), Compendium of the microbiological spoilage of foods and beverages (pp. 87-119). Springer.
Houicher, A., Bensid, A., Regenstein, J. M., & Ozogul, F. (2021). Control of biogenic amine production and bacterial growth in fish and seafood products using phytochemicals as biopreservatives: A review. Food Bioscience, 39, 100807. https://doi.org/10.1016/j.fbio.2020.100807
Jay, J. M., Loessner, M. J., & Golden, D. A. (2005). Processed meats and seafoods. In J. M. Jay, M. J. Loessner & D. A. Golden (Eds.). Modern food microbiology (7. ed., pp. 101-124). Springer. https://doi.org/10.1007/0-387-23413-6_5
Jia, S., Liu, Y., Zhuang, S., Sun, X., Li, Y., Hong, H., Lv, Y., & Luo, Y. (2019). Effect of ε-polylysine and ice storage on microbiota composition and quality of Pacific white shrimp (Litopenaeus vannamei) stored at 0°C. Food Microbiology, 83, 27-35. https://doi.org/10.1016/j.fm.2019.04.007
Kanki, M., Yoda, T., Ishibashi, M., & Tsukamoto, T. (2004). Photobacterium phosphoreum caused a histamine fish poisoning incident. International Journal of Food Microbiology, 92(1), 79-87. https://doi.org/10.1016/j.ijfoodmicro.2003.08.019
Lakshmanan, R., Shakila, R., & Jeyasekaran, G. (2002). Survival of amine-forming bacteria during the ice storage of fish and shrimp. Food Microbiology, 19(6), 617-625. https://doi.org/10.1006/fmic.2002.0481
Lehane, L., & Lewis, R. J. (2000). Ciguatera: recent advances but the risk remains. International Journal of Food Microbiology, 61(2-3), 91-125. https://doi.org/10.1016/S0168-1605(00)00382-2
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550. https://doi.org/10.1186/s13059-014-0550-8
Martini, S., Al Ali, B., Garel, M., Nerini, D., Grossi, V., Pacton, M., Casalot, L., Cuny, P., & Tamburini, C. (2013). Effects of hydrostatic pressure on growth and luminescence of a moderately-piezophilic luminous bacterium Photobacterium phosphoreum ANT-2200. PLoS One, 8(6), e66580. https://doi.org/10.1371/journal.pone.0066580
Ministério da Agricultura e Pecuária (MAPA) (2019). Government eliminates import tariffs on sardines for one year. MAPA. Retrieved from https://www.gov.br/agricultura/pt-br/assuntos/noticias/governo-reduz-tarifade-importacao-de-sardinha-a-zero-por-um-ano
Ministério da Agricultura e Pecuária (MAPA) (2020). Regulation of Industrial and Sanitary Inspection of Animal Products (RIISPOA). MAPA.
Moi, I. M., Roslan, N. N., Leow, A. T. C., Ali, M. S. M., Rahman, R. N. Z. R. A., Rahimpour, A., & Sabri, S.(2017). The biology and importance of Photobacterium species. Applied Microbiology and Biotechnology, 101, 4371-4385. https://doi.org/10.1007/s00253-017-8300-y
Møretrø, T., & Langsrud, S. (2017). Residential bacteria on surfaces in the food industry and their implications for food safety and quality. Comprehensive Reviews in Food Science and Food Safety, 16(5), 1022-1041. https://doi.org/10.1111/1541-4337.12283
Møretrø, T., Moen, B., Heir, E., Hansen, A. A., & Langsrud, S. (2016). Contamination of salmon fillets and processing plants with spoilage bacteria. International Journal of Food Microbiology, 237, 98-108. https://doi.org/10.1016/j.ijfoodmicro.2016.08.016
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., & Wagner, H. (2019). Vegan: Community Ecology Package. R package version 2.5-5. Retrieved from https://CRAN.R-project.org/package=vegan
Oku, N., Kawabata, K., Adachi, K., Katsuta, A., & Shizuri, Y. (2008). Unnarmicins A and C, new antibacterial depsipeptides produced by marine bacterium Photobacterium sp. MBIC06485. Journal of Antibiotics, 61, 11-17. https://doi.org/10.1038/ja.2008.103
Parrilli, E., Tedesco, P., Fondi, M., Tutino, M. L., Giudice, A., Pascale, D., & Fani, R. (2021). The art of adapting to extreme environments: The model system Pseudoalteromonas. Physics of Life Reviews, 36, 137-161. https://doi.org/10.1016/j.plrev.2019.04.003
Peivasteh-Roudsari, L., Rahmani, A., Shariatifar, N., Tajdar-Oranj, B., Mazaheri, M., Sadighara, P., & Khaneghah, A. M. (2020). Occurrence of histamine in canned fish samples (tuna, sardine, kilka, and mackerel) from markets in Tehran. Journal of Food Protection, 83(1), 136-141. https://doi.org/10.4315/0362-028X.JFP-19-288
Rio, B., Fernandez, M., Redruello, B., Ladero, V., & Alvarez, M. A. (2024). New insights into the toxicological effects of dietary biogenic amines. Food Chemistry, 435, 137558. https://doi.org/10.1016/j.foodchem.2023.137558
Rossano, R., Mastrangelo, L., Ungaro, N., & Riccio, P. (2006). Influence of storage temperature and freezing time on histamine level in the European anchovy Engraulis encrasicholus (L., 1758): a study by capillary electrophoresis. Journal of Chromatography B, 830(1), 161-164. https://doi.org/10.1016/j.jchromb.2005.10.026
Saelens, G., & Houf, K. (2022). Systematic review and critical reflection on the isolation and identification methods for spoilage associated bacteria in fresh marine fish. Journal of Microbiological Methods, 203, 106599. https://doi.org/10.1016/j.mimet.2022.106599
Takahashi, H., Ogai, M., Miya, S., Kuda, T., & Kimura, B. (2015). Effects of environmental factors on histamine production in the psychrophilic histamineproducing bacterium Photobacterium iliopiscarium. Food Control, 52, 39-42. https://doi.org/10.1016/j.foodcont.2014.12.023
Thompson, F. L., & Swings, J. (2006). Taxonomy of the Vibrios. In F. L. Thompson, B. Austin & J. Swings (Eds.), The Biology of Vibrios (pp. 29-43). ASM Press. https://doi.org/10.1128/9781555815714
Wang, Y., Naumann, U., Eddelbuettel, D., Wilshire, J., Warton, D., Byrnes, J., Silva, V. S., Niku, J., Renner, I., & Wright, S. (2022). mvabund: Statistical Methods for Analysing Multivariate Abundance Data. R package version 4.0.1. Retrieved from https://CRAN.R-project.org/package=mvabund
Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag.
Yang, X. (2014). Moraxellaceae. In G. W. Smithers (Ed.), Encyclopedia of Food Microbiology (2. ed., pp. 826-833). Academic Press. https://doi.org/10.1016/B978-0-12-384730-0.00441-9
Downloads
Published
Issue
Section
License
Copyright (c) 2024 Luca Frondana, Daniel da Rosa Farias, Delano Dias Schleder
This work is licensed under a Creative Commons Attribution 4.0 International License.