Identification of Bacterial Species from Fermented Anchovy (Engraulis encrasicolus) Samples by MALDI-TOF MS and Determination of Some Microbiological Properties of These Samples

Öz

Türkiye is a country surrounded by sea on three sides. Therefore, it is very rich in terms of seafood; however, unfortunately, fermented seafood is not very common in our country. Fermented anchovy (Engraulis encrasicolus) is traditionally produced in some villages and/or local provinces of the Black Sea Region. In this study, two traditionally fermented anchovy (Engraulis encrasicolus) samples obtained from Artvin and Trabzon were used. Characteristic colonies isolated from these samples were identified via MALDI-TOF MS. Moreover, total mesophilic aerobic bacteria, total lactic acid bacteria (LAB), and total yeast and mold of these samples were also determined. Bacillus thuringiensis, Bacillus subtilis, and Paenibacillus pabuli were identified in the Trabzon sample, whereas Micrococcus luteus and Bacillus simplex were identified in the Artvin sample by MALDI-TOF MS. Moreover, Artvin sample had the more total lactic acid bacteria (LAB), total mesophilic aerobic bacteria, and total yeast and mold than Trabzon sample. This study aims to increase awareness of fermented seafood in our country, and some microbiological properties of these fermented anchovy samples were revealed.

Anahtar Kelimeler

• Fermented anchovy
• MALDI-TOF MS
• total mesophilic aerobic bacteria
• total lactic acid bacteria
• total yeast and mold

Kaynakça

1. Alan, Y. (2019). Culture fermentation of Lactobacillus in traditional pickled gherkins: Microbial development, chemical, biogenic amine and metabolite analysis. Journal of Food Science and Technology, 56(8), 3930–3939. https://doi.org/10.1007/s13197-019-03866-8
2. Alan, Y., Topalcengiz, Z., & Dığrak, M. (2018). Biogenic amine and fermentation metabolite production assessments of Lactobacillus plantarum isolates for naturally fermented pickles. LWT, 98(11), 322–328. https://doi.org/10.1016/j.lwt.2018.08.067
3. Babio, N., Becerra-Tomás, N., Martínez-González, M. Á., Corella, D., Estruch, R., Ros, E., . . . Salas-Salvadó, J. (2015). Consumption of Yogurt, Low-Fat Milk, and Other Low-Fat Dairy Products Is Associated with Lower Risk of Metabolic Syndrome Incidence in an Elderly Mediterranean Population. The Journal of Nutrition, 145(10), 2308–2316. https://doi.org/10.3945/jn.115.214593
4. Bartoszewicz, M., Hansen, B. M., & Swiecicka, I. (2008). The members of the Bacillus cereus group are commonly present contaminants of fresh and heat-treated milk. Food Microbiology, 25(4), 588–596. https://doi.org/10.1016/j.fm.2008.02.001
5. Chuon, M. R., Shiomoto, M., Koyanagi, T., Sasaki, T., Michihata, T., Chan, S., . . . Enomoto, T. (2014). Microbial and chemical properties of Cambodian traditional fermented fish products. Journal of the Science of Food and Agriculture, 94(6), 1124–1131. https://doi.org/10.1002/jsfa.6379
6. Damgaard, P. H., Larsen, H. D., Hansen, B. M., Bresciani, J., & Jørgensen, K. (1996). Enterotoxin-producing strains of Bacillus thuringiensis isolated from food. Letters in Applied Microbiology, 23(3), 146–150. https://doi.org/10.1111/j.1472-765x.1996.tb00051.x
7. Eom, J. S., Lee, S. Y., & Choi, H. S. (2014). Bacillus subtilis HJ18-4 from traditional fermented soybean food inhibits Bacillus cereus growth and toxin-related genes. Journal of Food Science, 79(11), M2279-87. https://doi.org/10.1111/1750-3841.12569
8. Erkmen, O., Erten, H., & Sağlam, H. (2020). Fermente Ürünler Teknolojisi ve Mikrobiyolojisi. Ankara, Türkiye: Nobel Akademik Yayıncılık Eğitim Danışmanlık Tic. Ltd. Şti.

9. FAO (2024). The State of World Fisheries and Aquaculture 2024. Retrieved from https://openknowledge.fao.org/server/api/core/bitstreams/66538eba-9c85-4504-8438-c1cf0a0a3903/content/sofia/2024/world-fisheries-aquaculture-production.html
10. Galvez, A., Lopez, R. L., Abriouel, H., Valdivia, E., & Omar, N. B. (2008). Application of bacteriocins in the control of foodborne pathogenic and spoilage bacteria. Critical Reviews in Biotechnology, 28(2), 125–152. https://doi.org/10.1080/07388550802107202
11. Jemil, I., Jridi, M., Nasri, R., Ktari, N., Ben Slama-Ben Salem, R., Mehiri, M., . . . Nasri, M. (2014). Functional, antioxidant and antibacterial properties of protein hydrolysates prepared from fish meat fermented by Bacillus subtilis A26. Process Biochemistry, 49(6), 963–972. https://doi.org/10.1016/j.procbio.2014.03.004
12. Kaya, Y., Duyar, H. A., & Erdem, M. E. (2004). Balık Yağ Asitlerinin İnsan Sağlığı İçin Önemi. Ege Üniversitesi Su Ürünleri Dergisi, 21(3-4), 365–370.
13. Kılınç, B., & Çaklı, Ş. (2021). Production of dry fermented fish sausages by using different fish species and determination of the microbiological qualities. Ege Journal of Fisheries and Aquatic Sciences, 38(3), 329–336. https://doi.org/10.12714/egejfas.38.3.09
14. Kobayashi, T., Okuzumi, M., & Fujii, T. (1995). Microflora of Fermented Puffer Fish Ovaries in Rice-Bran “Fugunoko Nukazuke”. Fisheries Science, 61(2), 291–295. https://doi.org/10.2331/fishsci.61.291
15. Larsson, S. C., Andersson, S.-O., Johansson, J.-E., & Wolk, A. (2008). Cultured milk, yogurt, and dairy intake in relation to bladder cancer risk in a prospective study of Swedish women and men. The American Journal of Clinical Nutrition, 88(4), 1083–1087. https://doi.org/10.1093/ajcn/88.4.1083
16. Le Duc, H., Dong, T. C., Logan, N. A., Sutherland, A. D., Taylor, J., & Cutting, S. M. (2005). Cases of emesis associated with bacterial contamination of an infant breakfast cereal product. International Journal of Food Microbiology, 102(2), 245–251. https://doi.org/10.1016/j.ijfoodmicro.2004.11.022
17. Li, G., Li, X., Dong, L., Li, C., Zou, P., Saleemi, M. K., . . . Xu, Y. (2021). Isolation, Identification and Characterization of Paenibacillus pabuli E1 to Explore Its Aflatoxin B1 Degradation Potential. Current Microbiology, 78(10), 3686–3695. https://doi.org/10.1007/s00284-021-02624-4
18. Mohd Isa, M. H., Shamsudin, N. H., Al-Shorgani, N. K. N., Alsharjabi, F. A., & Kalil, M. S. (2020). Evaluation of antibacterial potential of biosurfactant produced by surfactin-producing Bacillus isolated from selected Malaysian fermented foods. Food Biotechnology, 34(1), 1–24. https://doi.org/10.1080/08905436.2019.1710843
19. Mondal, M., Tewari, S., Mukherjee, P. A., & Khalua, R. K. (2022). A REVIEW ON FERMENTED FISH: MICROBIOLOGY, CHEMISTRY AND HEALTH BENEFITS. Journal of Population and Therapeutics and Clinical Pharmacology. Advance online publication. https://doi.org/10.53555/jptcp.v29i04.2888
20. Park, K. M., Kim, H. J., Jeong, M. C., & Koo, M. (2016). Occurrence of Toxigenic Bacillus cereus and Bacillus thuringiensis in Doenjang, a Korean Fermented Soybean Paste. Journal of Food Protection, 79(4), 605–612. https://doi.org/10.4315/0362-028X.JFP-15-416
21. Park, S., & Bae, J.-H. (2016). Fermented food intake is associated with a reduced likelihood of atopic dermatitis in an adult population (Korean National Health and Nutrition Examination Survey 2012-2013). Nutrition Research (New York, N.Y.), 36(2), 125–133. https://doi.org/10.1016/j.nutres.2015.11.011
22. Rezac, S., Kok, C. R., Heermann, M., & Hutkins, R. (2018). Fermented Foods as a Dietary Source of Live Organisms. Frontiers in Microbiology, 9, 1785. https://doi.org/10.3389/fmicb.2018.01785
23. Stein, T., Heinzmann, S., Düsterhus, S., Borchert, S., & Entian, K.-D. (2005). Expression and functional analysis of the subtilin immunity genes spaIFEG in the subtilin-sensitive host Bacillus subtilis MO1099. Journal of Bacteriology, 187(3), 822–828. https://doi.org/10.1128/JB.187.3.822-828.2005
24. Tanasupawat, S., Hashimoto, Y., Ezaki, T., Kozaki, M., & Komagata, K. (1992). Staphylococcus piscifermentans sp. Nov., from fermented fish in Thailand. International Journal of Systematic Bacteriology, 42(4), 577–581. https://doi.org/10.1099/00207713-42-4-577
25. Tanasupawat, S., & Daengsubha, W. (1983). Pediococcus species and related bacteria found in fermented foods and related materials in Thailand. The Journal of General and Applied Microbiology, 29, 487–506.
26. Tanasupawat, S., Ezaki, T., Suzuki, K.-I., Okada, S., Komagata, K., & Kozaki, M. (1992). Characterization and identification of Lactobacillus pentosus and Lactobacillus plantarum strains from fermented foods in Thailand. The Journal of General and Applied Microbiology, 38(2), 121–134. https://doi.org/10.2323/jgam.38.121
27. Tanasupawat, S., Hashimoto, Y., Ezaki, T., Kozaki, M., & Komagata, K. (1991). Identification of staphylococcus carnosus strains from fermented fish and soy sauce mash. The Journal of General and Applied Microbiology, 37(6), 479–494. https://doi.org/10.2323/jgam.37.479
28. Tanasupawat, S., Okada, S., & Komagata, K. (1998). Lactic acid bacteria found in fermented fish in Thailand. The Journal of General and Applied Microbiology, 44(3), 193–200. https://doi.org/10.2323/jgam.44.193
29. Torino, M. I., Limón, R. I., Martínez-Villaluenga, C., Mäkinen, S., Pihlanto, A., Vidal-Valverde, C., & Frias, J. (2013). Antioxidant and antihypertensive properties of liquid and solid state fermented lentils. Food Chemistry, 136(2), 1030–1037. https://doi.org/10.1016/j.foodchem.2012.09.015
30. Uysal, A. (2019). Doğu Akdeniz Bölgesi’nde Turunçgillerde Antraknoz Etmeni Colletotrichum Türlerinin Morfolojik, Patojenik, Moleküler Karakterizasyonu ve Fungisit Duyarlılıkları (Doctoral Thesis). Hatay Mustafa Kemal University, Hatay, Türkiye.
31. Yeo, I.-C., Lee, N. K., & Hahm, Y. T. (2012). Genome sequencing of Bacillus subtilis SC-8, antagonistic to the Bacillus cereus group, isolated from traditional Korean fermented-soybean food. Journal of Bacteriology, 194(2), 536–537. https://doi.org/10.1128/JB.06442-11
32. Zaman, M. Z., Bakar, F. A., Selamat, J., & Bakar, J. (2010). Occurrence of biogenic amines and amines degrading bacteria in fish sauce. Czech Journal of Food Sciences, 28(5), 440–449. https://doi.org/10.17221/312/2009-CJFS