Insights into microbiota community dynamics and flavor development mechanism during golden pomfret (<i>Trachinotus ovatus</i>) fermentation based on single-molecule real-time sequencing and molecular networking analysis

Yueqi Wang; Qian Chen; Huan Xiang; Dongxiao Sun-Waterhouse; Shengjun Chen; Yongqiang Zhao; Laihao Li; Yanyan Wu

doi:10.26599/FSHW.2022.9250008

Food Science and Human Wellness 2024, 13(1): 101-114 https://doi.org/10.26599/FSHW.2022.9250008

Research Article |

Open Access | Issue | Published: 01 June 2023

Insights into microbiota community dynamics and flavor development mechanism during golden pomfret (Trachinotus ovatus) fermentation based on single-molecule real-time sequencing and molecular networking analysis

Show Author's Information Hide Author's Information Yueqi Wang^{^a^,^b^,^d}, Qian Chen^{^a}, Huan Xiang^{^a^,^b^,^d}, Dongxiao Sun-Waterhouse^{^a^,^c}, Shengjun Chen^{^a^,^b^,^d}, Yongqiang Zhao^{^a^,^b^,^d}, Laihao Li^{^a^,^b^,^d}, Yanyan Wu^{^a^,^b^,^d^,}(

)

Key Laboratory of Aquatic Product Processing, Ministry of Agriculture and Rural Affairs of The People’s Republic of China, National R&D Center for Aquatic Product Processing, South China Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510300, China

Co-Innovation Center of Jiangsu Marine Bio-industry Technology, Jiangsu Ocean University, Lianyungang 222005, China

School of Chemical Sciences, The University of Auckland, Auckland 92019, New Zealand

Collaborative Innovation Center of Seafood Deep Processing, Dalian Polytechnic University, Dalian 116034, China

Peer review under responsibility of Tsinghua University Press.

Keywords:

Co-occurrence network, Fermented golden pomfret, Microbiota community, Volatile compound, Metabolic pathway

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Wang Y, Chen Q, Xiang H, et al. Insights into microbiota community dynamics and flavor development mechanism during golden pomfret (Trachinotus ovatus) fermentation based on single-molecule real-time sequencing and molecular networking analysis. Food Science and Human Wellness, 2024, 13(1): 101-114. https://doi.org/10.26599/FSHW.2022.9250008

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Abstract Full text Electronic supplementary material About this article

Abstract

Popular fermented golden pomfret (Trachinotus ovatus) is prepared via spontaneous fermentation; however, the mechanisms underlying the regulation of its flavor development remain unclear. This study shows the roles of the complex microbiota and the dynamic changes in microbial community and flavor compounds during fish fermentation. Single-molecule real-time sequencing and molecular networking analysis revealed the correlations among different microbial genera and the relationships between microbial taxa and volatile compounds. Mechanisms underlying flavor development were also elucidated via KEGG based functional annotations. Clostridium, Shewanella, and Staphylococcus were the dominant microbial genera. Forty-nine volatile compounds were detected in the fermented fish samples, with thirteen identified as characteristic volatile compounds (ROAV > 1). Volatile profiles resulted from the interactions among the microorganisms and derived enzymes, with the main metabolic pathways being amino acid biosynthesis/metabolism, carbon metabolism, and glycolysis/gluconeogenesis. This study demonstrated the approaches for distinguishing key microbiota associated with volatile compounds and monitoring the industrial production of high-quality fermented fish products.

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Insights into microbiota community dynamics and flavor development mechanism during golden pomfret (Trachinotus ovatus) fermentation based on single-molecule real-time sequencing and molecular networking analysis

Show Author's information Hide Author's Information Yueqi Wang^{^a^,^b^,^d}, Qian Chen^{^a}, Huan Xiang^{^a^,^b^,^d}, Dongxiao Sun-Waterhouse^{^a^,^c}, Shengjun Chen^{^a^,^b^,^d}, Yongqiang Zhao^{^a^,^b^,^d}, Laihao Li^{^a^,^b^,^d}, Yanyan Wu^{^a^,^b^,^d^,}(

)

Co-Innovation Center of Jiangsu Marine Bio-industry Technology, Jiangsu Ocean University, Lianyungang 222005, China

School of Chemical Sciences, The University of Auckland, Auckland 92019, New Zealand

Collaborative Innovation Center of Seafood Deep Processing, Dalian Polytechnic University, Dalian 116034, China

Peer review under responsibility of Tsinghua University Press.

Highlights

• Fermentation in golden pomfret shows varied microbiota and flavor changes over time.

• Clostridium, Shewanella, and Staphylococcus were the dominant genera detected.

• Thirteen compounds were identified as key flavor components in fermented golden pomfret.

• Amino acid metabolism, lipid metabolism and carbohydrate metabolism were the main metabolic pathway.

• The mechanisms associated with the flavor formation were illuminated.

Abstract

Keywords: Co-occurrence network, Fermented golden pomfret, Microbiota community, Volatile compound, Metabolic pathway

References(41)

[1]

Q. Chen, Y. Wang, Y. Wu, et al., Investigation of fermentation-induced changes in the volatile compounds of Trachinotus ovatus (Meixiangyu) based on molecular sensory and interpretable machine-learning techniques: Comparison of different fermentation stages, Food Res. Int. 150 (2021) 110739. https://doi.org/10.1016/j.foodres.2021.110739.

DOI Google Scholar

[2]

X. Zeng, W. Xia, Q. Jiang, et al., Contribution of mixed starter cultures to flavor profile of suanyu: a traditional Chinese low-salt fermented whole fish, J. Food Process. Preserv. 41 (2017) 15. https://doi.org/10.1111/jfpp.13131.

DOI Google Scholar

[3]

H. Xiang, D. Sun-Waterhouse, G.I.N. Waterhouse, et al., Fermentationenabled wellness foods: A fresh perspective, Food Sci. Hum. Wellness. 8(2019) 203-243. https://doi.org/10.1016/j.fshw.2019.08.003.

DOI Google Scholar

[4]

M. Ongmu Bhutia, N. Thapa, H. Nakibapher Jones Shangpliang, et al., Metataxonomic profiling of bacterial communities and their predictive functional profiles in traditionally preserved meat products of Sikkim state in India, Food Res. Int. 140 (2021) 110002. https://doi.org/10.1016/j.foodres.2020.110002.

DOI Google Scholar

[5]

F. An, M. Li, Y. Zhao, et al., Metatranscriptome-based investigation of flavor-producing core microbiota in different fermentation stages of dajiang, a traditional fermented soybean paste of Northeast China, Food Chem. 343(2021) 128509. https://doi.org/10.1016/j.foodchem.2020.128509.

DOI Google Scholar

[6]

Y. Wang, C. Li, Y. Zhao, et al., Novel insight into the formation mechanism of volatile flavor in Chinese fish sauce (Yu-lu) based on molecular sensory and metagenomics analyses, Food Chem. 323 (2020) https://doi.org/10.10.1016/j.foodchem.2020.126839.

DOI Google Scholar

[7]

Q. Peng, S. Jiang, J. Chen, et al., Unique microbial diversity and metabolic pathway features of fermented vegetables from hainan, China, Front Microbiol. 9 (2018). https://doi.org/10.3389/fmicb.2018.00399.

DOI Google Scholar

[8]

J. Zang, Y. Xu, W. Xia, et al., Dynamics and diversity of microbial community succession during fermentation of Suan yu, a Chinese traditional fermented fish, determined by high throughput sequencing, Food Res. Int. 111 (2018) 565-573. https://doi.org/10.1016/j.foodres.2018.05.076.

DOI Google Scholar

[9]

Z. Wang, Z. Xu, L. Sun, et al., Dynamics of microbial communities, texture and flavor in Suan zuo yu during fermentation, Food Chem. 332 (2020) 127364. https://doi.org/10.1016/j.foodchem.2020.127364.

DOI Google Scholar

[10]

C. Zhao, J. Eun, Shotgun metagenomics approach reveals the bacterial community and metabolic pathways in commercial hongeo product, a traditional Korean fermented skate product, Food Res. Int. 131 (2020) 109030. https://doi.org/10.1016/j.foodres.2020.109030.

DOI Google Scholar

[11]

E. Reynisson, H.L. Lauzon, H. Magnusson, et al., Bacterial composition and succession during storage of North-Atlantic cod (Gadus morhua) at superchilled temperatures, Bmc Microbiol. 9 (2009). https://doi.org/10.1186/1471-2180-9-250.

DOI Google Scholar

[12]

X. Lou, D. Zhai, H. Yang, Changes of metabolite profiles of fish models inoculated with Shewanella baltica during spoilage, Food Control. 123 (2021) 107697. https://doi.org/10.1016/j.foodcont.2020.107697.

DOI Google Scholar

[13]

J. Liang, D. Li, R. Shi, et al., Effects of microbial community succession on volatile profiles and biogenic amine during sufu fermentation, LWT-Food Sci. Technol. 114 (2019) 108379. https://doi.org/10.1016/j.lwt.2019.108379

DOI Google Scholar

[14]

M. Rabie, L. Simon-Sarkadi, H. Siliha, et al., Changes in free amino acids and biogenic amines of Egyptian salted-fermented fish (Feseekh) during ripening and storage, Food Chem. 115 (2009) 635-638. https://doi.org/10.1016/j.foodchem.2008.12.077.

DOI Google Scholar

[15]

A. Giri, K. Osako, T. Ohshima, Identification and characterisation of headspace volatiles of fish miso, a Japanese fish meat based fermented paste, with special emphasis on effect of fish species and meat washing, Food Chem. 120 (2010) 621-631.10.1016/j. foodchem. 2009.10.036.

DOI Google Scholar

[16]

G. Fratini, S. Lois, M. Pazos, et al., Volatile profile of Atlantic shellfish species by HS-SPME GC/MS, Food Res. Int. 48 (2012) 856-865. https://doi.org/10.1016/j.foodres.2012.06.033.

DOI Google Scholar

[17]

W. Zhu, H. Luan, Y. Bu, et al., Flavor characteristics of shrimp sauces with different fermentation and storage time, LWT-Food Sci. Technol. 110 (2019) 142-151. https://doi.org/10.1016/j.lwt.2019.04.091.

DOI Google Scholar

[18]

L. Cano-García, S. Rivera-Jiménez, C. Belloch, et al., Generation of aroma compounds in a fermented sausage meat model system by Debaryomyces hansenii strains, Food Chem. 151 (2014) 364-373. https://doi.org/10.1016/j.foodchem.2013.11.051.

DOI Google Scholar

[19]

S. Landaud, S. Helinck, P. Bonnarme, Formation of volatile sulfur compounds and metabolism of methionine and other sulfur compounds in fermented food, Appl. Microbiol. Biotechnol. 77 (2008) 1191-1205. https://doi.org/10.1007/s00253-007-1288-y.

DOI Google Scholar

[20]

C. LI, J. Wu., Y. Li, et al., Identification of the aroma compounds in stinky mandarin fish (Siniperca chuatsi) and comparison of volatiles during fermentation and storage, Int. J. Food Sci. Technol. 48 (2013) 2429-2437. https://doi.org/10.1111/ijfs.12254.

DOI Google Scholar

[21]

Y. Hu, L. Zhang, H. Zhang, et al., Physicochemical properties and flavour profile of fermented dry sausages with a reduction of sodium chloride, LWT-Food Sci. Technol. 124 (2020) 109061. https://doi.org/10.1016/j.lwt.2020.109061.

DOI Google Scholar

[22]

A. Giri, K. Osako, A. Okamoto, et al., Olfactometric characterization of aroma active compounds in fermented fish paste in comparison with fish sauce, fermented soy paste and sauce products, Food Res. Int. 43 (2010) 1027-1040. https://doi.org/10.1016/j.foodres.2010.01.012.

DOI Google Scholar

[23]

Q. Chen, B. Kong, Q. Han, et al., The role of bacterial fermentation in lipolysis and lipid oxidation in Harbin dry sausages and its flavour development, LWT-Food Sci. Technol. 77 (2017) 389-396. https://doi.org/10.1016/j.lwt.2016.11.075.

DOI Google Scholar

[24]

J. Luo, C.B. Jiang, L. Zhao, et al., Keto acid decarboxylase and keto acid dehydrogenase activity detected during the biosynthesis of flavor compound 3-methylbutanal by the nondairy adjunct culture Lactococcus lactis ssp lactis F9, J. Dairy Sci. 101 (2018) 9725-9735. https://doi.org/10.3168/jds.2018-14760.

DOI Google Scholar

[25]

A. Ding, M. Zhu, X. Qian, et al., Effect of fatty acids on the flavor formation of fish sauce, LWT-Food Sci. Technol. 134 (2020) https://doi.org/10.1016/j.lwt.2020.110259.

DOI Google Scholar

[26]

Arief. Ⅱ, D.N. Afiyah, Z. Wulandari, et al., Physicochemical properties, fatty acid profiles, and sensory characteristics of fermented beef sausage by probiotics Lactobacillus plantarum IIA-2C12 or Lactobacillus acidophilus IIA-2B4, J. Food Sci. 81 (2016) M2761-M2769. https://doi.org/10.1111/1750-3841.13509.

DOI Google Scholar

[27]

Q. Zhao, Q. Shen, R. Guo, et al., Characterization of flavor properties from fish (Collichthys niveatus) through enzymatic hydrolysis and the Maillard reaction, J. Aquat. Food Prod. Technol. 25 (2016) 482-495. https://doi.org/10.1080/10498850.2013.873965.

DOI Google Scholar

[28]

Y. Shen, Y. Wu, Y. Wang, et al., Contribution of autochthonous microbiota succession to flavor formation during Chinese fermented mandarin fish (Siniperca chuatsi), Food Chem. 348 (2021) 129107. https://doi.org/10.1016/j.foodchem.2021.129107.

DOI Google Scholar

[29]

L. Cai, Z. Ao, T. Tang, et al., Characterization of difference in muscle volatile compounds between triploid and diploid crucian carp, Aquacult. Rep. 20 (2021) 100641. https://doi.org/10.1016/j.aqrep.2021.100641.

DOI Google Scholar

[30]

J. Yang, J. Lu, Q. Zhu, et al., Isolation and characterization of a novel Lactobacillus plantarum MMB-07 from traditional Suanyu for Acanthogobius hasta fermentation, J. Biosci. Bioeng. (2021). https://doi.org/10.1016/j.jbiosc.2020.12.016.

DOI Google Scholar

[31]

X. Zhou, Y. Chong, Y. Ding, et al., Determination of the effects of different washing processes on aroma characteristics in silver carp mince by MMSE-GC-MS, e-nose and sensory evaluation, Food Chem. 207 (2016) 205-213. https://doi.org/10.1016/j.foodchem.2016.03.026.

DOI Google Scholar

[32]

K.M. Prashant, T. Jyoti, G. Sumit, et al., GC-MS olfactometric characterization of odor active compounds in cooked red kidney beans (Phaseolus vulgaris), Heliyon. 5 (2019). https://doi.org/10.1016/j.heliyon.2019.e02459.

DOI Google Scholar

[33]

G. Yao, J. Yu, Q. Hou, et al., A perspective study of koumiss microbiome by metagenomics analysis based on single-cell amplification technique, Front Microbiol. 8 (2017). https://doi.org/10.3389/fmicb.2017.00165.

DOI Google Scholar

[34]

D. Zhang, H.W. Ji, S.C. Liu, et al., Similarity of aroma attributes in hotair-dried shrimp (Penaeus vannamei) and its different parts using sensory analysis and GC-MS, Food Res. Int. 137 (2020) 109517. https://doi.org/10.1016/j.foodres.2020.109517.

DOI Google Scholar

[35]

X. Huang, S. Yu, B. Han, et al., Bacterial community succession and metabolite changes during sufu fermentation, LWT-Food Sci. Technol. 97(2018) 537-545. https://doi.org/10.1016/j.lwt.2018.07.041.

DOI Google Scholar

[36]

S. Liu, Q. Chen, H. Zou, et al., A metagenomic analysis of the relationship between microorganisms and flavor development in Shaoxing mechanized huangjiu fermentation mashes, Int. J. Food Microbiol. 303 (2019) 9-18. https://doi.org/10.1016/j.ijfoodmicro.2019.05.001

DOI Google Scholar

[37]

D. Liu, C. Zhang, J. Zhang, et al., Metagenomics reveals the formation mechanism of flavor metabolites during the spontaneous fermentation of potherb mustard (Brassica juncea var. multiceps), Food Res. Int. (2021) 110622. https://doi.org/10.1016/j.foodres.2021.110622.

DOI Google Scholar

[38]

B.A. Smit, W.J.M. Engels, G. Smit, Branched chain aldehydes: production and breakdown pathways and relevance for flavour in foods, Appl. Microbiol. Biotechnol. 81 (2009) 987-999. https://doi.org/10.1007/s00253-008-1758-x.

DOI Google Scholar

[39]

Y. Wang, Y. Shen, Y. Wu, et al., Comparison of the microbial community and flavor compounds in fermented mandarin fish (Siniperca chuatsi): Three typical types of Chinese fermented mandarin fish products, Food Res. Int. (2021) 110365. Https://doi.org/10.1016/j.foodres.2021.110365.

DOI Google Scholar

[40]

X. Luo, S. Xiao, Q. Ruan, et al., Differences in flavor characteristics of frozen surimi products reheated by microwave, water boiling, steaming, and frying, Food Chem. 372 (2022) 131260. https://doi.org/10.1016/j.foodchem.2021.131260.

DOI Google Scholar

[41]

J.E. Cronan, J. Thomas, Bacterial fatty acid synthesis and its relationships with polyketide synthetic pathways, in: D.A. Hopwood (Ed.), Complex Enzymes in Microbial Natural Product Biosynthesis, Part B: Polyketides, Aminocoumarins and Carbohydrates, 2009, 395-433.

DOI Google Scholar

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Received: 14 April 2022

Revised: 26 May 2022

Accepted: 22 June 2022

Published: 01 June 2023

Issue date: January 2024

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (32001733), the Earmarked fund for CARS (CARS-47), Guangxi Natural Science Foundation Program (2021GXNSFAA196023), Guangdong Basic and Applied Basic Research Foundation (2021A1515010833), Young Talent Support Project of Guangzhou Association for Science and Technology (QT20220101142) and the Special Scientific Research Funds for Central Non-profit Institutes, Chinese Academy of Fishery Sciences (2020TD69).

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