Correlation between the bacterial community and flavour of fermented fish
Main Article Content
Keywords
fermented fish, bacterial community, flavour
Abstract
Common carp is a fish species of economic importance in China;traditionally it is mostly salt-fermented. In the fermenting process, the bacterial community of spontaneously fermented fish is important for its flavour and quality. However, very few studies have been conducted about the relationship between bacterial community and development of flavour involved in the salt-fermentation of carp. Therefore, we explored this relationship by determining the flavour components, including amino acids, and changes in volatile flavour and bacterial metabolite. Samples were taken during fermentation on the days 0, 10, 20, 30, 40 and 50. The second-generation 16S recombinant DNA (rDNA) sequencing was performed to analyze the composition of bacteria. Contents of amino acids were determined by reverse-phase high-performance liquid chromatography combined with ultraviolet detection. The volatile components were analyzed with solid-phase microextraction–gas chromatography-mass spectrometry. Enterococcus, Lactobacillus, Lactococcus, Leuconostoc, and Staphylococcus were the dominant bacteria. The bidirectional orthogonal partial least squares approach was used to analyze the correlation between bacterial succession and flavour component dynamics. This study would help to better understand the role of bacteria in the fermented fish meat flavour and support the industrial production of fermented fish.
References
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Dong, F., 2015. Serum metabolomics study of polycystic ovary syndrome based on UPLC-QTOF-MS coupled with a pattern recognition approach. Analytical and Bioanalytical Chemistry 407: 4683–4695. 10.1007/s00216-015-8670-x
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Gao, P., Wang, W.X., Jiang, Q.X., Xu, Y.S. and Xia, W.S., 2016a. Effect of autochthonous starter cultures on the volatile flavour compounds of Chinese traditional fermented fish (Suan yu). International Journal of Food Science and Technology 51(7): 1630–1637. 10.1111/ijfs.13134
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Ma, J., Li, Y., Chen, H., Zeng, Z., Li, Z.-L. and Jiang, H., 2016. Synthesis of oxylipin mimics and their antifungal activity against the citrus postharvest pathogens. Molecules 21(2): 254. 10.3390/molecules21020254
Martin, A., Colin, B., Aranda, E., Benito, M.J. and Cordoba, M.G., 2007. Characterization of Micrococcaceae isolated from Iberian dry-cured sausages. Meat Science 75(4): 696–708. 10.1016/j.meatsci.2006.10.001
Marui, J., Boulom, S. and Panthavee, W., 2014. Culture-independent analysis of the bacterial community during fermentation of pa-som, a traditional fermented fish product in Laos. Fisheries Science 80: 1109–1115. 10.1007/s12562-014-0780-4
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Ojha, K.S., Kerry, J.P., Duffy, G., Beresford, T. and Tiwari, B.K., 2015. Technological advances for enhancing quality and safety of fermented meat products. Trends in Food Science and Technology 44(1): 105–116. 10.1016/j.tifs.2015.03.010
Ozogul Y, İlknur Yuvka, Ucar Y, Durmus M, Kösker AR, Öz M, Ozogul F, 2017. Evaluation of effects of nanoemulsion based on herb essential oils (rosemary, laurel, thyme and sage) on sensory, chemical and microbiological quality of rainbow trout (Oncorhynchus mykiss) fillets during ice storage, LWT-Food Science and Technology 75: 677–684. 10.1016/j.lwt.2016.10.009
Paludan-Müller, C., Madsen, M. and Sophanodora, P., 2002. Fermentation and microflora of plaa-som, a Thai fermented fish product prepared with different salt concentrations. International Journal of Food Microbiology 73: 61–70. 10.1016/S0168-1605(01)00688-2
Pang X.N., Han B.Z. and Huang X.N., 2018. Effect of the environment microbiota on the flavour of light-flavour Baijiu during spontaneous fermentation. Scientfic Report 8: 3396. 10.1038/s41598-018-21814-y
Quijada, N.M., De Filippis, F., Sanz, J. J., García-Fernández, M.d. C., Rodríguez-Lázaro, D., Ercolini, D. and Hernández, M., 2017. High-throughput sequencing analysis reveals different lactobacillus populations that dominate during “Chorizo de León” cured meat making. Food Microbiology 70: 94–102. 10.1016/j.fm.2017.09.009
Riquelme, C., Câmara, S., Enes Dapkevicius, M.-N., Vinuesa, P., da Silva, C.-G., 2015. Characterization of the bacterial biodiversity in Pico cheese (an artisanal Azorean food). International Journal of Food Microbiology 192: 86–94. 10.1016/j.ijfoodmicro.2014.09.031
Ruiz-Moyano, S., Martin, A., Benito, M.J., Hernandez, A., Casquete, R. and de Guia Cordoba, M., 2011. Application of Lactobacillus fermentum HL57 and Pediococcus acidilactici SP979 as potential probiotics in the manufacture of traditional Iberian dry-fermented sausages. Food Microbiology 28: 839–847. 10.1016/j.fm.2011.01.006
Sallam, K.I., 2007. Chemical, sensory and shelf life evaluation of sliced salmon treated with salts of organic acids. Food Chemistry 101: 592–600. 10.1016/j.foodchem.2006.02.019
Soto Del Rio, M.L.D., Dalmasso, A., Civera, T. and Bottero, M.T., 2017. Characterization of bacterial communities of donkey milk by high-throughput sequencing. International Journal of Food Microbiology 251: 67–72. 10.1016/j.ijfoodmicro.2017.03.023
Stergaard, A., Embarek, P.K.B. and Yamprayoon, J., 1998. Fermentation and spoilage of som fak, a Thai low-salt fish product. Tropical Science 38: 105–112.
Takahashi H. and Kimura, B., 2010. Comparison of PCR-DGGE and PCR-SSCP analysis for bacterial flora of Japanese traditional fermented fish products, aji-narezushi and iwashi-nukazuke. Journal of the Science of Food and Agriculture 90: 1796–1801.
Trygg, J., 2002. O2-PLS for qualitative and quantitative analysis in multivariate calibration. Journal of Chemometrics 16: 283–293. 10.1002/cem.724
Wang, Y., 2012. Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Applied and Environmental Microbiology 78: 8264–8271. 10.1128/AEM.01821-12
Wang, Q., Garrity, G.M., Tiedje, J.M. and Cole, J.R., 2007. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73: 5261–5267. 10.1128/AEM.00062-07
Wang Y., Jiang Y.T. and Cao, J.X., 2016. Study on lipolysis-oxidation and volatile flavour compounds of dry-cured goose with different curing salt content during production. Food Chemistry 190: 33–40. 10.1016/j.foodchem.2015.05.048
Wang, W.X., Xia, W.S. and Xu, Y.S., 2014. Research progress on quality and safety of traditional solid-state fermentation freshwater fish. Journal of Food Safety and Quality 5: 1093–1099.
Wolfe, B.E., Button, J.E., Santarelli, M. and Dutton, R.J., 2014. Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell 158: 422. 10.1016/j.cell.2014.05.041
Wolfe, B.E. and Dutton, R.J., 2015. Fermented foods as experimentally tractable microbial ecosystems. Cell 161: 49. 10.1016/j.cell.2015.02.034
Xiong, J., 2012. Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan plateau. Environmental Microbiology 14: 2457–2466. 10.1111/j.1462-2920.2012.02799.x
Xu, Y., Li, L., Regenstein, J.M., Gao, P., Zang, J., Xia, W., Jiang, Q., 2018. The contribution of autochthonous microflora on free fatty acids release and flavour development in low-salt fermented fish. Food Chemistry 256: 259–267. 10.1016/j.foodchem.2018.02.142
Yin L.J., Pan C.L. and Jiang S.T., 2002a. Effect of lactic acid bacterial fermentation on the characteristics of minced mackerel. Journal of Food Science 67: 786–792. 10.1111/j.1365-2621.2002.tb10677.x
Yin L.J., Pan C.L. and Jiang S.T., 2002b. New technology for producing paste-like fish products using lactic acid bacteria fermentation. Journal of Food Science 67: 3114–3118. 10.1111/j.1365-2621.2002.tb08867.x
Yu M.J., Tan H. and Ma M.H., 2017. Bacterial community diversity and quality characteristics in traditional solid-fermented fish. Food Science 38(8): 86–95 (in Chinese with English abstract).
Zang J.H., Yu D.W., Xu Y.S., Yang F., Gao P. Xia W.S. and Jiang Q.X., 2018. Dynamics and diversity of microbial community succession during fermentation of Suan yu, a Chinese traditional fermented fish, determined by high throughput sequencing. Food Research International 111: 565–573. 10.1016/j.foodres.2018.05.076
Zeng, X. F., Chen, X. H. and Zhang, W., 2016. Characterization of the microbial flora from Suan Yu, a Chinese traditional low-salt fermented fish. Journal of Food Processing and Preservation, 40(5): 1093–1103. 10.1111/jfpp.12690
Zeng, X., Xia, W., Jiang, Q. and Yang, F., 2013. Effect of autochthonous starter cultures on microbiological and physico-chemical characteristics of Suan yu, a traditional Chinese low-salt fermented fish. Food Control 33(2): 344–351. 10.1016/j.foodcont.2013.03.001
Zhang H., Li Y., Xu K., Wu J. and Dai Z., 2015. Microbiological changes and biodiversity of cultivable indigenous bacteria in Sanbao larger yellow croaker (Pseudosciaena crocea), a Chinese salted and fermented seafood. Journal of Food Science 80(4): M776–M781. 10.1111/1750-3841.12818
Zheng X.J., Liu F. Shi X.W., Wang B., Li K.X., Li B.K. and Zhuge B., 2018 March. Dynamic correlations between microbiota succession and flavour development involved in the ripening of Kazak artisanal cheese. Food Research International 105: 733–742. 10.1016/j.foodres.2017.12.007
Benito, M.J., Rodriguez, M., Cordoba, M.G., Andrade, M.J. and Cordoba, J.J., 2005. Effect of the fungal protease EPg222 on proteolysis and texture in the dry fermented sausage ‘salchichón’. Journal of the Science of Food and Agriculture 85: 273–280. 10.1002/jsfa.1951
Beriain, M., Horcada, A., Purroy, A., Lizaso, G., Chasco, J. and Mendizabal, J., 2000. Characteristics of lacha and rasa aragonesa lambs slaughtered at three live weights. Journal of Animal Science 78: 3070–3077. 10.2527/2000.78123070x
Bolumar, T., Nieto, P., Flores, J., 2001. Acidity, Proteolysis and lipolysis changes in rapid-cured fermented sausage dried at different temperatures. Food Science and Technology International 7: 269–276. 10.1177/108201301772660240
Bylesjö, M., Eriksson, D., Kusano, M., Moritz, T. and Trygg, J., 2007. Data integration in plant biology: the O2PLS method for combined modeling of transcript and metabolite data. Plant Journal 52: 1181–1191. 10.1111/j.1365-313X.2007.03293.x
Carpino, S., Randazzo, C.L., Pino, A., Russo, N. and Rapisarda, T., 2017. Influence of PDO Ragusano cheese biofilm microbiota on flavour compounds formation. Food Microbiology 61: 126–135. 10.1016/j.fm.2016.09.006
Casaburi, A., Aristoy, M.C., Cavella, S., Di M.R., Ercolini, D., Toldra, F. and Villani, F., 2007. Biochemical and sensory characteristics of traditional fermented sausages of Vallo di Diano (Southern Italy) as affected by the use of starter cultures. Meat Science 76: 295–307. 10.1016/j.meatsci.2006.11.011
Dai, Z., Li, Y., Wu, J. and Zhao, Q., 2013. Diversity of lactic acid bacteria during fermentation of a traditional Chinese fish product, chouguiyu (stinky mandarin fish). Journal of Food Science 78(11): 1778–1783. 10.1111/1750-3841.12289
De Filippis, F., Genovese, A., Ferranti, P., Gilbert, J.A. and Ercolini, D., 2015. Metatranscriptomics reveals temperature-driven functional changes in microbiome impacting cheese maturation rate. Scientific Reports 6: 21871. 10.1038/srep21871
Dong, F., 2015. Serum metabolomics study of polycystic ovary syndrome based on UPLC-QTOF-MS coupled with a pattern recognition approach. Analytical and Bioanalytical Chemistry 407: 4683–4695. 10.1007/s00216-015-8670-x
Ercolini, D., De Filippis, F., La Storia, A. and Iacono, M., 2012. “Remake” by high-throughput sequencing of the microbiota involved in the production of water buffalo mozzarella cheese. Appl. Environ. Microbiol 78: 8142–8145. 10.1128/AEM.02218-12
Escobar-Zepeda, A., Sanchez-Flores, A. and Baruch, M.Q., 2016. Metagenomic analysis of a Mexican ripened cheese reveals a unique complex microbiota. Food Microbiology 57: 116–127. 10.1016/j.fm.2016.02.004
Gao, P., Wang, W.X., Jiang, Q.X., Xu, Y.S. and Xia, W.S., 2016a. Effect of autochthonous starter cultures on the volatile flavour compounds of Chinese traditional fermented fish (Suan yu). International Journal of Food Science and Technology 51(7): 1630–1637. 10.1111/ijfs.13134
Ji, C.F., Zhang J.B., Lin X.P., Han, J., Dong X.P., Yang, S., Yan, X.M. and Zhu B.W., 2017. Metaproteomic analysis of microbiota in the fermented fish, Siniperca chuatsi. LWT—Food Science and Technology 80: 479–484. 10.1016/j.lwt.2017.03.022
Jung, J.Y., Lee, S.H., Lee, H.J. and Jeon, C.O., 2013. Microbial succession and metabolite changes during fermentation of saeu-jeot: traditional Korean salted seafood. Food Microbiology 34(2): 360–368. 10.1016/j.fm.2013.01.009
Kouakou, A.C., Guessan, K.F. and Durand, N., 2012. Molecular bacterial characterization and free amino acids composition in Ivorian traditional fermented fish produced by two methods. Fisheries Science 78: 1125–1136. 10.1007/s12562-012-0526-0
Koyanagi, T., 2011. Pyrosequencing survey of the microbial diversity of ‘narezushi’, an archetype of modern Japanese sushi. Letters in Applied Microbiology 53: 635–640. 10.1111/j.1472-765X.2011.03155.x
Kuda, T., Tanibe, R., Mori, M., Take, H., Michihata, T., Yano, T., Takahashi, H. and Kimura, B., 2009. Microbial and chemical properties of aji-no-susu, a traditional fermented fish with rice product in the Noto Peninsula, Japan. Fisheries Science 75(6): 1499–1506. 10.1007/s12562-009-0175-0
Ma, J., Li, Y., Chen, H., Zeng, Z., Li, Z.-L. and Jiang, H., 2016. Synthesis of oxylipin mimics and their antifungal activity against the citrus postharvest pathogens. Molecules 21(2): 254. 10.3390/molecules21020254
Martin, A., Colin, B., Aranda, E., Benito, M.J. and Cordoba, M.G., 2007. Characterization of Micrococcaceae isolated from Iberian dry-cured sausages. Meat Science 75(4): 696–708. 10.1016/j.meatsci.2006.10.001
Marui, J., Boulom, S. and Panthavee, W., 2014. Culture-independent analysis of the bacterial community during fermentation of pa-som, a traditional fermented fish product in Laos. Fisheries Science 80: 1109–1115. 10.1007/s12562-014-0780-4
Nie, Z., Zheng, Y., Xie, S., Zhang, X., Song, J., Xia, M. and Wang, M., 2017. Unraveling the correlation between microbiota succession and metabolite changes in traditional Shanxi aged vinegar. Sci. Rep. 7: 9240. 10.1038/s41598-017-09850-6
Ojha, K.S., Kerry, J.P., Duffy, G., Beresford, T. and Tiwari, B.K., 2015. Technological advances for enhancing quality and safety of fermented meat products. Trends in Food Science and Technology 44(1): 105–116. 10.1016/j.tifs.2015.03.010
Ozogul Y, İlknur Yuvka, Ucar Y, Durmus M, Kösker AR, Öz M, Ozogul F, 2017. Evaluation of effects of nanoemulsion based on herb essential oils (rosemary, laurel, thyme and sage) on sensory, chemical and microbiological quality of rainbow trout (Oncorhynchus mykiss) fillets during ice storage, LWT-Food Science and Technology 75: 677–684. 10.1016/j.lwt.2016.10.009
Paludan-Müller, C., Madsen, M. and Sophanodora, P., 2002. Fermentation and microflora of plaa-som, a Thai fermented fish product prepared with different salt concentrations. International Journal of Food Microbiology 73: 61–70. 10.1016/S0168-1605(01)00688-2
Pang X.N., Han B.Z. and Huang X.N., 2018. Effect of the environment microbiota on the flavour of light-flavour Baijiu during spontaneous fermentation. Scientfic Report 8: 3396. 10.1038/s41598-018-21814-y
Quijada, N.M., De Filippis, F., Sanz, J. J., García-Fernández, M.d. C., Rodríguez-Lázaro, D., Ercolini, D. and Hernández, M., 2017. High-throughput sequencing analysis reveals different lactobacillus populations that dominate during “Chorizo de León” cured meat making. Food Microbiology 70: 94–102. 10.1016/j.fm.2017.09.009
Riquelme, C., Câmara, S., Enes Dapkevicius, M.-N., Vinuesa, P., da Silva, C.-G., 2015. Characterization of the bacterial biodiversity in Pico cheese (an artisanal Azorean food). International Journal of Food Microbiology 192: 86–94. 10.1016/j.ijfoodmicro.2014.09.031
Ruiz-Moyano, S., Martin, A., Benito, M.J., Hernandez, A., Casquete, R. and de Guia Cordoba, M., 2011. Application of Lactobacillus fermentum HL57 and Pediococcus acidilactici SP979 as potential probiotics in the manufacture of traditional Iberian dry-fermented sausages. Food Microbiology 28: 839–847. 10.1016/j.fm.2011.01.006
Sallam, K.I., 2007. Chemical, sensory and shelf life evaluation of sliced salmon treated with salts of organic acids. Food Chemistry 101: 592–600. 10.1016/j.foodchem.2006.02.019
Soto Del Rio, M.L.D., Dalmasso, A., Civera, T. and Bottero, M.T., 2017. Characterization of bacterial communities of donkey milk by high-throughput sequencing. International Journal of Food Microbiology 251: 67–72. 10.1016/j.ijfoodmicro.2017.03.023
Stergaard, A., Embarek, P.K.B. and Yamprayoon, J., 1998. Fermentation and spoilage of som fak, a Thai low-salt fish product. Tropical Science 38: 105–112.
Takahashi H. and Kimura, B., 2010. Comparison of PCR-DGGE and PCR-SSCP analysis for bacterial flora of Japanese traditional fermented fish products, aji-narezushi and iwashi-nukazuke. Journal of the Science of Food and Agriculture 90: 1796–1801.
Trygg, J., 2002. O2-PLS for qualitative and quantitative analysis in multivariate calibration. Journal of Chemometrics 16: 283–293. 10.1002/cem.724
Wang, Y., 2012. Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Applied and Environmental Microbiology 78: 8264–8271. 10.1128/AEM.01821-12
Wang, Q., Garrity, G.M., Tiedje, J.M. and Cole, J.R., 2007. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73: 5261–5267. 10.1128/AEM.00062-07
Wang Y., Jiang Y.T. and Cao, J.X., 2016. Study on lipolysis-oxidation and volatile flavour compounds of dry-cured goose with different curing salt content during production. Food Chemistry 190: 33–40. 10.1016/j.foodchem.2015.05.048
Wang, W.X., Xia, W.S. and Xu, Y.S., 2014. Research progress on quality and safety of traditional solid-state fermentation freshwater fish. Journal of Food Safety and Quality 5: 1093–1099.
Wolfe, B.E., Button, J.E., Santarelli, M. and Dutton, R.J., 2014. Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell 158: 422. 10.1016/j.cell.2014.05.041
Wolfe, B.E. and Dutton, R.J., 2015. Fermented foods as experimentally tractable microbial ecosystems. Cell 161: 49. 10.1016/j.cell.2015.02.034
Xiong, J., 2012. Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan plateau. Environmental Microbiology 14: 2457–2466. 10.1111/j.1462-2920.2012.02799.x
Xu, Y., Li, L., Regenstein, J.M., Gao, P., Zang, J., Xia, W., Jiang, Q., 2018. The contribution of autochthonous microflora on free fatty acids release and flavour development in low-salt fermented fish. Food Chemistry 256: 259–267. 10.1016/j.foodchem.2018.02.142
Yin L.J., Pan C.L. and Jiang S.T., 2002a. Effect of lactic acid bacterial fermentation on the characteristics of minced mackerel. Journal of Food Science 67: 786–792. 10.1111/j.1365-2621.2002.tb10677.x
Yin L.J., Pan C.L. and Jiang S.T., 2002b. New technology for producing paste-like fish products using lactic acid bacteria fermentation. Journal of Food Science 67: 3114–3118. 10.1111/j.1365-2621.2002.tb08867.x
Yu M.J., Tan H. and Ma M.H., 2017. Bacterial community diversity and quality characteristics in traditional solid-fermented fish. Food Science 38(8): 86–95 (in Chinese with English abstract).
Zang J.H., Yu D.W., Xu Y.S., Yang F., Gao P. Xia W.S. and Jiang Q.X., 2018. Dynamics and diversity of microbial community succession during fermentation of Suan yu, a Chinese traditional fermented fish, determined by high throughput sequencing. Food Research International 111: 565–573. 10.1016/j.foodres.2018.05.076
Zeng, X. F., Chen, X. H. and Zhang, W., 2016. Characterization of the microbial flora from Suan Yu, a Chinese traditional low-salt fermented fish. Journal of Food Processing and Preservation, 40(5): 1093–1103. 10.1111/jfpp.12690
Zeng, X., Xia, W., Jiang, Q. and Yang, F., 2013. Effect of autochthonous starter cultures on microbiological and physico-chemical characteristics of Suan yu, a traditional Chinese low-salt fermented fish. Food Control 33(2): 344–351. 10.1016/j.foodcont.2013.03.001
Zhang H., Li Y., Xu K., Wu J. and Dai Z., 2015. Microbiological changes and biodiversity of cultivable indigenous bacteria in Sanbao larger yellow croaker (Pseudosciaena crocea), a Chinese salted and fermented seafood. Journal of Food Science 80(4): M776–M781. 10.1111/1750-3841.12818
Zheng X.J., Liu F. Shi X.W., Wang B., Li K.X., Li B.K. and Zhuge B., 2018 March. Dynamic correlations between microbiota succession and flavour development involved in the ripening of Kazak artisanal cheese. Food Research International 105: 733–742. 10.1016/j.foodres.2017.12.007
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