PDF (3 MB)
Collect
Submit Manuscript
Show Outline
Figures (5)

Open Access

Changes in microorganisms and metabolites during long-term fermentation of commercially manufactured anchovy sauce

Dae-Hyun KimaSeong-Eun ParkaEun-Ju KimaSeung-Ho SeobKwang-Moon ChocKwon Sun-JaecHong-Seok Sona()
Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University, Seoul 02841, Korea
Sonlab Inc., Seoul 02841, Korea
AccuGene Inc., Incheon 21999, Korea

Peer review under responsibility of Beijing Academy of Food Sciences.

Show Author Information

Highlights

• Changes in microbial communities and metabolites during the long-term fermentation of commercially manufactured anchovy sauce were investigated.

Tetragenococcus and Halanaerobium were dominant genera in commercial anchovy sauce after 0.55 years of fermentation.

• Most of the metabolites present in anchovy sauce were produced within 1 year of fermentation.

• This study provides insights into long-term changes in microbiota and metabolites in fish sauce produced without starter inoculation.

Graphical Abstract

View original image Download original image

Abstract

This study was performed to investigate the changes in microbial communities and metabolites during the long-term fermentation of commercially manufactured anchovy sauce. Samples of commercial anchovy sauce were collected from large-scale fermentation tanks with fermentation periods of up to 7.87 years. The complex bacterial community was simplified to two genera, Tetragenococcus and Halanaerobium, after approximately 0.55 years of fermentation. Although genera, such as Saccharomyces, Cladosporium, Candida, and Aspergillus, were relatively dominant, no clear pattern was identified in fungal community analysis. The longitudinal metabolite profile demonstrated that approximately half (55.8%) of the metabolites present in anchovy sauce were produced within a year of fermentation due to rapid fermentation. Despite the static microbial community, the contents of several metabolites including amino acids and biogenic amines changed continuously during the long-term fermentation of anchovy sauce. This study provides novel insights into the changes in microbiota and metabolites in fish sauce produced without any starter inoculation.

Electronic Supplementary Material

Download File(s)
fshw-14-1-9250014_ESM.docx (4.4 MB)

References

[1]

S.H. Hur, Critical review on the microbiological standardization of salt-fermented fish product, J. Korean Soc. Food Sci. Nutr. 25 (1996) 885-891.

[2]
KOSIS. Fisheries Processing Industry Statistics. Retrieved from https://kosis.kr/statHtml/statHtml.do?orgId=146&tblId=DT_MLTM_5002733&conn_path=I2. Accessed November 14, 2022.
[3]

S.M. Lee, A.K. Asaduzzaman, B.S. Chun, Characterization of lecithin isolated from anchovy (Engraulis japonica) residues deoiled by supercritical carbon dioxide and organic solvent extraction, J. Food Sci. 77 (2012) C773-778. https://doi.org/10.1111/j.1750-3841.2012.02764.x.

[4]

H.W Lee, Y.J. Choi, I.M. Hwang, et al., Relationship between chemical characteristics and bacterial community of a Korean salted-fermented anchovy sauce, Myeolchi-Aekjeot, LWT-Food Sci. Technol. 73 (2016) 251-258. https://doi.org/10.1016/j.lwt.2016.06.007.

[5]

K. Fukami, Y. Funatsu, K. Kawasaki, et al., Improvement of fish-sauce odor by treatment with bacteria isolated from the fish-sauce mush (Moromi) made from frigate mackerel, J. Food Sci. 69 (2006) fms45-fms49. https://doi.org/10.1111/j.1365-2621.2004.tb15514.x.

[6]

J. Yongsawatdigul, S. Rodtong, N. Raksakulthai, Acceleration of Thai fish sauce fermentation using proteinases and bacterial starter cultures, J. Food Sci. 72 (2007) M382-M390. https://doi.org/10.1111/j.1750-3841.2007.00532.x.

[7]

Y.S. Lim, B.J. You, Y.J. Choi, et al., Difference of components changes in salt-fermented anchovy, Engraulis japonicus sauce by tank size during fermentation, Korean J. Fish Aquat. Sci. 35 (2002) 302-307. https://doi.org/10.5657/kfas.2002.35.3.302.

[8]

Y. J. Cho, Y.S. Im, H.Y. Park, et al., Changes of components in salt-fermented anchovy, Engraulis japonicus sauce during fermentation, Korean J. Fish Aquat. Sci. 33 (2000) 9-15.

[9]

S.H. Lee, J.Y. Jung, C.O. Jeon, Bacterial community dynamics and metabolite changes in myeolchi-aekjeot, a Korean traditional fermented fish sauce, during fermentation, Food Microbiol. 203 (2015) 15-22. https://doi.org/10.1016/j.ijfoodmicro.2015.02.031.

[10]

K.H. Nam, M.S. Jang, H.Y. Park, Component changes in commercial salt-fermented anchovy sauce by long fermentation, J. Agric. Life Sci. 46 (2012) 99-107.

[11]

S.H. Lee, J.Y. Jung, C.O. Jeon, Effects of temperature on microbial succession and metabolite change during saeu-jeot fermentation, Food Microbiol. 38 (2014) 16-25. https://doi.org/10.1016/j.fm.2013.08.004.

[12]

R. Margesin, F. Schinner, Potential of halotolerant and halophilic microorganisms for biotechnology, Extremophiles 5 (2001) 73-83. https://doi.org/10.1007/s007920100184.

[13]

N. Udomsil, S. Rodtong, S. Tanasupawat, et al., Proteinase-producing halophilic lactic acid bacteria isolated from fish sauce fermentation and their ability to produce volatile compounds, Int. J. Food Microbiol. 141 (2010) 186-194. https://doi.org/10.1016/j.ijfoodmicro.2010.05.016.

[14]

Y. Fukui, M. Yoshida, K. Shozen, et al., Bacterial communities in fish sauce mash using culture-dependent and -independent methods, J. Appl. Microbiol. 58 (2012) 273-281. https://doi.org/10.2323/jgam.58.273.

[15]

W. Taira, Y. Funatsu, M. Satomi, et al., Changes in extractive components and microbial proliferation during fermentation of fish sauce from underutilized fish species and quality of final products, Fish Sci. 73 (2007) 913-923. https://doi.org/10.1111/j.1444-2906.2007.01414.x.

[16]

L. Guan, K.H. Cho, J.H. Lee, Analysis of the cultivable bacterial community in jeotgal, a Korean salted and fermented seafood, and identification of its dominant bacteria, Food Microbiol. 28 (2011) 101-113. https://doi.org/10.1016/j.fm.2010.09.001.

[17]

M.S. Kim, E.J. Park, Bacterial communities of traditional salted and fermented seafoods from Jeju Island of Korea using 16S rRNA gene clone library analysis, J. Food Sci. 79 (2014) M927-M934. https://doi.org/10.1111/1750-3841.12431.

[18]

J.Y. Jung, H.J. Lee, B.H. Chun, et al., Effects of temperature on bacterial communities and metabolites during fermentation of Myeolchi-Aekjeot, a traditional Korean fermented anchovy sauce, PLoS One 11 (2016) e0151351. https://doi.org/10.1371/journal.pone.0151351.

[19]

K. Ihrmark, I.T.M. Bödeker, K. Cruz-Martinez, et al., New primers to amplify the fungal ITS2 region: evaluation by 454-sequencing of artificial and natural communities, FEMS Microbiol. Ecol. 82 (2012) 666-677. https://doi.org/10.1111/j.1574-6941.2012.01437.x.

[20]

A.E. Parada, D.M. Needham, J.A. Fuhrman, Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples, Environ. Microbiol. 18 (2016) 1403-1414. https://doi.org/10.1111/1462-2920.13023.

[21]

B.J. Callahan, P.J. McMurdie, M.J. Rosen, et al., DADA2: high-resolution sample inference from Illumina amplicon data, Nat. Methods 13 (2016) 581-583. https://doi.org/10.1038/nmeth.3869.

[22]

F.O. Glöckner, P. Yilmaz, C. Quast, et al., 25 years of serving the community with ribosomal RNA gene reference databases and tools, J. Biotechnol. 261 (2017) 169-176. https://doi.org/10.1016/j.jbiotec.2017.06.1198.

[23]

E. Bolyen, J.R. Rideout, M.R. Dillon, et al., Reproducible, interactive, scalable and extensible microbiome data science using QⅡME 2, Nat. Biotechnol. 37 (2019) 852-857. https://doi.org/10.1038/s41587-019-0209-9.

[24]

V. Shulaev, Metabolomics technology and bioinformatics, Brief. Bioinformatics 7 (2006) 128-139. https://doi.org/10.1093/bib/bbl012.

[25]

O.A. Adebo, S.A. Oyeyinka, J.A. Adebiyi, et al., Application of gas chromatography-mass spectrometry (GC-MS)-based metabolomics for the study of fermented cereal and legume foods: a review, Int. J. Food Sci. Technol. 56 (2021) 1514-1534. https://doi.org/10.1111/ijfs.14794.

[26]

S.H. Lee, J.Y. Jung, C.O. Jeon, Microbial successions and metabolite changes during fermentation of salted shrimp (saeu-jeot) with different salt concentrations, PLoS One 9 (2014) e90115. https://doi.org/10.1371/journal.pone.0090115.

[27]

J.R. López, J.I. Navas, N. Thanantong, et al., Simultaneous identification of five marine fish pathogens belonging to the genera Tenacibaculum, Vibrio, Photobacterium and Pseudomonas by reverse line blot hybridization, Aquaculture 324 (2012) 33-38. https://doi.org/10.1016/j.aquaculture.2011.10.043.

[28]
P. Saisithi, Traditional fermented fish: fish sauce production. in: A.M. Martin (Ed.), Fisheries Processing, Springer, 1994, pp. 111-131. https://doi.org/10.1007/978-1-4615-5303-8_5.
[29]

T. Kobayashi, M. Kajiwara, M. Wahyuni, et al., Effect of culture conditions on lactic acid production of Tetragenococcus species, J. Appl. Microbiol. 96 (2004) 1215-1221. https://doi.org/10.1111/j.1365-2672.2004.02267.x.

[30]

B. Kimura, Y. Konagaya, T. Fujii, Histamine formation by Tetragenococcus muriaticus, a halophilic lactic acid bacterium isolated from fish sauce, Int. J. Food Microbiol. 70 (2001) 71-77. https://doi.org/10.1016/S0168-1605(01)00514-1.

[31]

M. Satomi, K. Shozen, A. Furutani, et al., Analysis of plasmids encoding the tyrosine decarboxylase gene in Tetragenococcus halophilus isolated from fish sauce, Fish Sci. 80 (2014) 849-858. https://doi.org/10.1007/s12562-014-0756-4.

[32]

J. Sitdhipol, S. Tanasupawat, P. Tepkasikulet, et al., Identification and histamine formation of Tetragenococcus isolated from Thai fermented food products, Ann. Microbiol. 63 (2013) 745-753. https://doi.org/10.1007/s13213-012-0529-1.

[33]

C. Li, W. Li, L. Li, et al., Microbial community changes induced by a newly isolated salt-tolerant Tetragenococcus muriaticus improve the volatile flavor formation in low-salt fish sauce, Food Res. Int. 156 (2022) 111153. https://doi.org/10.1016/j.foodres.2022.111153.

[34]

N. Udomsil, S. Chen, S. Rodtong, et al., Improvement of fish sauce quality by combined inoculation of Tetragenococcus halophilus MS33 and Virgibacillus sp. SK37, Food Control 73 (2017) 930-938. https://doi.org/10.1016/j.foodcont.2016.10.007.

[35]

N. Udomsil, S. Rodtong, Y.J. Choi, et al., Use of Tetragenococcus halophilus as a starter culture for flavor improvement in fish sauce fermentation, J. Agric. Food Chem. 59 (2011) 8401-8408. https://doi.org/10.1021/jf201953v.

[36]

J.Y. Jung, S.H. Lee, H.J. Lee, et al., Microbial succession and metabolite changes during fermentation of saeu-jeot: traditional Korean salted seafood, Food Microbiol. 34 (2013) 360-368. https://doi.org/10.1016/j.fm.2013.01.009.

[37]
T.C. Bhalla, Savitri, Yeasts and traditional fermented foods and beverages. In: T. Satyanarayana, G. Kunze (Eds.), Yeast Diversity in Human Welfare. Springer, Singapore, 2017, pp. 53-82. https://doi.org/10.1007/978-981-10-2621-8.
[38]

M.M. Abdel-Kareem, A.M. Rasmey, A.A. Zohri, The action mechanism and biocontrol potentiality of novel isolates of Saccharomyces cerevisiae against the aflatoxigenic Aspergillus flavus, Lett. Appl. Microbiol. 68 (2019) 104-111. https://doi.org/10.1111/lam.13105.

[39]

E.J. Kim, S.H. Seo, S.E. Park, et al., Initial storage of kimchi at room temperature alters its microbial and metabolite profiles, LWT-Food Sci. Technol. 134 (2020) 110160. https://doi.org/10.1016/j.lwt.2020.110160.

[40]

S. Wold, K. Esbensen, P. Geladi, Principal component analysis, Chemometr Intell. Lab. Syst. 2 (1987) 37-52. https://doi.org/10.1016/0169-7439(87)80084-9.

[41]

Ö. Özden, Changes in amino acid and fatty acid composition during shelf-life of marinated fish, J. Sci. Food Agric. 85 (2005) 2015-2020. https://doi.org/10.1002/jsfa.2207.

[42]

B.S. Sivamaruthi, P. Kesika, C. Chaiyasut, A narrative review on biogenic amines in fermented fish and meat products, J. Food Sci. Technol. 58 (2021) 1623-1639. https://doi.org/10.1007/s13197-020-04686-x.

[43]

J. Han, T. Kong, Q. Wang, et al., Regulation of microbial metabolism on the formation of characteristic flavor and quality formation in the traditional fish sauce during fermentation: a review, Crit. Rev. Food Sci. Nutr. 63(25) (2022) 7564-7583. https://doi.org/10.1080/10408398.2022.2047884.

[44]

X. MA, J. Bi, X. Li, et al., Contribution of microorganisms to biogenic amine accumulation during fish sauce fermentation and screening of novel starters, Foods 10 (2021) 2572. https://doi.org/10.3390/foods10112572.

[45]

G.V. de Melo Pereira, D.P. de Carvalho Neto, A.C.D.O. Junqueira, et al., A review of selection criteria for starter culture development in the food fermentation industry, Food Rev. Int. 36 (2020) 135-167. https://doi.org/10.1080/87559129.2019.1630636.

Food Science and Human Wellness
Article number: 9250014
Cite this article:
Kim D-H, Park S-E, Kim E-J, et al. Changes in microorganisms and metabolites during long-term fermentation of commercially manufactured anchovy sauce. Food Science and Human Wellness, 2025, 14(1): 9250014. https://doi.org/10.26599/FSHW.2024.9250014
Metrics & Citations  
Article History
Copyright
Rights and Permissions
Return