High-throughput sequencing approach to characterize dynamic changes of the fungal and bacterial communities during the production of sufu, a traditional Chinese fermented soybean food

Food Microbiology

Volumn 86, Issue , 2020, Pages

  Xu, Dandan ^a,b   Wang, Peng ^a,b   Zhang, Xin ^a   Zhang, Jian ^a,b   Sun, Yong ^a   Gao, Lihua ^a   Wang, Wenping ^a  

^a Beijing Academy of Food Sciences   (China)

^b Beijing Institute of Food and Brewing   (China)

Author keywords

Bacterial communities; Fermentation; Fungal communities; High throughput sequencing; Sufu

Indexed keywords

BACTERIUM; CLASSIFICATION; FERMENTATION; FUNGUS; GENETICS; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MICROFLORA; SOY FOOD; SOYBEAN;

BACTERIA; FERMENTATION; FUNGI; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICROBIOTA; SOY FOODS; SOYBEANS;

EID: 85072517099     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2019.103340     Document Type: Article

References (66)

1. Ammor, M.S., Mayo, B., 2007. Selection criteria for lactic acid bacteria to be used as functional starter cultures in dry sausage production: An update. Meat Sci. 76, 138-146.
2. Andersson, A., Ronner, U., Granum, P.E., 1995. What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens? Int. J. Food Microbio. 28, 145-155.
3. Blumenthal, C.Z., 2004. Production of toxic metabolites in Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei: justification of mycotoxin testing in food grade enzyme preparations derived from the three fungi. Regul Toxicol Pharm. 39, 214-228.
4. Breierova, E., Hromadkova, Z., Stratilova, E., Sasinkova, V., Ebringerova, A., 2005. Effect of salt stress on the production and properties of extracellular polysaccharides produced by Cryptococcus laurentii. Z Naturforsch C. 60, 444-450.
5. Cai, R.C., Li, L., Yang, M., Cheung, H.Y., Fu, L., 2016. Changes in bioactive compounds and their relationship to antioxidant activity in white sufu during manufacturing. Int. J. Food Sci. Tech. 51, 1721-1730.
6. Caporaso, J.G., Bittinger, K., Bushman, F.D., Desantis, T.Z., Andersen, G.L., Knight, R., 2009. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-267.
7. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, A.G., Goodrich, J.K., Gordon, J.I., 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336.
8. Chen, J., Quan, M.H., Cheng, Y.Q., Sun, J., Li, L.T., 2012. Acetylcholinesterase inhibitory activity of Chinese sufu (fermented tofu) ethanol-extract. Food Chem. 134, 1263-1266.
9. Chung, H.Y., Fung, P.K., Kim, J.S., 2005. Aroma impact components in commercial plain sufu. J. Agr. Food Chem. 53, 1684-1691.
10. Cole, J.R., Chai, B., Farris, R.J., Wang, Q., Kulam-syed-mohideen, A.S., Mcgarrell, D.M., Bandela, A.M., Cardenas, E., Garrity, G.M., Tiedje, J.M., 2006. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. 35, 169-172.
11. Colombo, A.L., Padovan, A.C.B., Chaves, G.M., 2011. Current knowledge of Trichosporon spp. and Trichosporonosis. Clin. Microbio. Rev. 24, 682-700.
12. DeSantis, T.Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E.L., Keller, K., Huber, T., Dalevi, D., Hu, P., Andersen, G.L., 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072.
13. Doughari, H.J., Ndakidemi, P.A., Human, I.S., Benade, S., 2011. The ecology, biology and pathogenesis of Acinetobacter spp.: an overview. Microbes Environ. 26, 101-112.
14. Drudy, D., O'Rourke, M., Murphy, M., Mullane, N.R., O'Mahony, R., Kelly, L., Fischer, M., Sanjaq, S., Shannon, P., Wall, P., 2006. Characterization of a collection of Enterobacter sakazakii isolates from environmental and food sources. Int. J. Food Microbiol. 110, 127-134.
15. Edgar, R.C., 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461.
16. Feng, Z., Gao, W., Ren, D., Chen, X., Li, J.J., 2013. Evaluation of bacterial flora during the ripening of Kedong sufu, a typical Chinese traditional bacteria-fermented soybean product. J. Sci. Food Agr. 93, 1471-1478.
17. Fields, M.L., Yoa, F.G., 1990. Nutritional improvement of corn meal by fermentation by Bacillus licheniformis and Enterobacter cloacae. J. Food Protect. 53, 245-248.
18. Granum, P.E., 1994. Bacillus cereus and its toxins. J. Appl. Bacteriol. 76, 61-66.
19. Han, B.Z., Cao, C.F., Rombouts, F.M., Nout, M.R., 2004. Microbial changes during the production of Sufu-a Chinese fermented soybean food. Food Control 15, 265-270.
20. Han, B.Z., Wang, J.H., Rombouts, F.M., Nout, M.R., 2003. Effect of NaCl on textural changes and protein and lipid degradation during the ripening stage of sufu, a Chinese fermented soybean food. J. Sci. Food Agr. 83, 899-904.
21. Hirokazu, T., Tanabe, A.S., Satoshi, Y., Hirotoshi, S., 2012. High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PloS one 7, e40863.
22. Hong, K.J., Lee, C.H., Kim, S.W., 2004. Aspergillus oryzae GB-107 fermentation improves nutritional quality of food soybeans and feed soybean meals. J. Med. Food 7, 430-435.
23. Hong, X., Chen, J., Lin, L., Wu, H., Tan, H., Xie, G., Xu, Q., Zou, H., Yu, W., Lan, W., Qin, N.,2016. Metagenomic sequencing reveals the relationship between microbiota composition and quality of Chinese Rice Wine. Sci. Rep-UK. 6, 26621.
24. Hu, C.W., Li, Q.Y., Zhou, C.H., Li, T.Q., Chen, J., Du, G.C., Fang, F., 2017. Functional analysis of bacteria isolated from soy sauce moromi. Microbio. China 44, 1899-1907.
25. Huang, C., Wu, H., Liu, Q.P., Li, Y.Y., Zong, M.H., 2011a. Effects of aldehydes on the growth and lipid accumulation of oleaginous yeast Trichosporon fermentans. J. Agr. Food Chem. 59, 4606-4613.
26. Huang, Y.H., Lai, Y.J., Chou, C.C., 2011b. Fermentation temperature affects the antioxidant activity of the enzyme-ripened sufu, an oriental traditional fermented product of soybean. J. Biosci. Bioeng. 112, 49-53.
27. Kang, J.H., Lee, J.H., Min, S., Min, D.B., 2006. Changes of volatile compounds, lactic acid bacteria, pH, and headspace gases in Kimchi, a traditional Korean fermented vegetable product. J. Food Sci. 68, 849-854.
28. Kilic, A.O., Pavlova, S.I., Ma, W.G., Tao, L., 1996. Analysis of Lactobacillus phages and bacteriocins in American dairy products and characterization of a phage isolated from yogurt. Appl. Environ. Microbiol. 62, 2111-2116.
29. Kim, H.R., Lee, A.R., Kim, J.H., 2017. Characteristics of Korean alcoholic beverages produced by using rice nuruks containing Aspergillus oryzae N159-1. Mycobiology 45, 119-122.
30. Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., Glockner, F. O., 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, e1-e1.
31. Li, Q., Li, Y., Luo, Y., Zhang, Y., Chen, Y., Lin, H., Wang, K., Huang, J., Liu, Z., 2019. Shifts in diversity and function of the bacterial community during the manufacture of Fu brick tea. Food Microbiol. 80, 70-76.
32. Li, Z., Dong, L., Huang, Q., Wang, X., 2016a. Bacterial communities and volatile compounds in Doubanjiang, a Chinese traditional red pepper paste. J. Appl. Microbiol. 120, 1585-1594.
33. Li, Z., HJ, A., NY, K., YN, L., GE, J., 2016b. Korean Ginseng berry fermented by mycotoxin Non-producing Aspergillus niger and Aspergillus oryzae: ginsenoside analyses and anti-proliferative activities. Biol. Pharm. Bull. 39, 1461-1467.
34. Li, Z., Rui, J., Li, X., Li, J., Dong, L., Huang, Q., Huang, C., Wang, Z., Li, L., Xuan, P., 2017. Bacterial community succession and metabolite changes during doubanjiang-meju fermentation, a Chinese traditional fermented broad bean (Vicia faba L.) paste. Food chem. 218, 534-542.
35. Liu, J., Han, B., Deng, S., Sun, S., Chen, J., 2018. Changes in proteases and chemical compounds in the exterior and interior of sufu, a Chinese fermented soybean food, during manufacture. LWT-Food Sci. Technol. 87, 210-216.
36. Lozupone, C.A., Knight, R., 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228-8235.
37. Ma, Y., Cheng, Y., Yin, L., Wang, J., Li, L., 2013a. Effects of processing and NaCl on angiotensin I-converting enzyme inhibitory activity and γ-aminobutyric acid content during Sufu manufacturing. Food Bioprocess Tech. 6, 1782-1789.
38. Ma, Y.L., Wang, J.H., Cheng, Y.Q., Yin, L.J., Li, L.T., 2013b. Some biochemical and physical changes during manufacturing of Grey Sufu, a traditional Chinese fermented soybean curd. Int. J. Food Eng. 9, 45-54.
39. Mao, X., Zhang, J., Kan, F., Gao, Y., Lan, J., Zhang, X., Hu, Z., Li, Y., Lin, H., 2013. Antioxidant production and chitin recovery from shrimp head fermentation with Streptococcus thermophilus. Food Sci. Biotechnol. 22, 1023-1032.
40. Masayuki, M., Osamu, Y., Katsuya, G., 2008. Genomics of Aspergillus oryzae: learning from the history of Koji mold and exploration of its future. DNA Res. 15, 173-183.
41. Moy, Y.S., Chou, C.C., 2010. Changes in the contents of sugars and organic acids during the ripening and storage of sufu, a traditional Oriental fermented product of soybean cubes. J. Agr. Food Chem. 58, 12790-12793.
42. Moy, Y.S., Lu, T.J., Chou, C.C., 2012. Volatile components of the enzyme-ripened sufu, a Chinese traditional fermented product of soy bean. J. Biosci. Bioeng. 113, 196-201.
43. Peleg, A.Y., Seifert, H., Paterson, D.L., 2008. Acinetobacter baumannii: emergence of a successful pathogen. Clin. Microbiol. Rev. 21, 538-582.
44. Price, M.N., Dehal, P.S., Arkin, A.P., 2009. FastTree: Computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641-1650.
45. Qiu, S., Wang, Y., Cheng, Y., Liu, Y., Yadav, M.P., Yin, L., 2018. Reduction of biogenic amines in sufu by ethanol addition during ripening stage. Food Chem. 239, 1244-1252.
46. Rocha, M.V.P., Oliveira, A.H.S., Souza, M.C.M., Goncalves, L.R.B., 2006. Natural cashew apple juice as fermentation medium for biosurfactant production by Acinetobacter calcoaceticus. World J. Microb. Biot. 22, 1295-1299.
47. Shen, Q., Lin, H., Zhan, J., Wang, Q., Zhao, Y., 2013. Sweetpotato vines hydrolysate induces glycerol to be an effective substrate for lipid production of Trichosporon fermentans. Bioresource Technol. 136, 725-729.
48. Shi, X.R., Fung, D.Y.C., 2000. Control of foodborne pathogens during sufu fermentation and aging. Crit. Rev. Food Sci. 40, 399-425.
49. Silva, C.F., Batista, L.R., Abreu, L.M., Dias, E.S., Schwan, R.F., 2008. Succession of bacterial and fungal communities during natural coffee (Coffea arabica) fermentation. Food Microbiol. 25, 951-957.
50. Song, Z., Du, H., Zhang, Y., Xu, Y., 2017. Unraveling core functional microbiota in traditional solid-state fermentation by high-throughput amplicons and metatranscriptomics sequencing. Front. Microbiol. 8, 1294.
51. Srianta, I., Ristiarini, S., Nugerahani, I., Sen, S.K., Zhang, B.B., Xu, G.R., Blanc, P.J., 2014. Recent research and development of Monascus fermentation products. Int. Food Res. J. 21, 1-12.
52. Sulaiman, J., Gan, H.M., Yin, W.F., Chan, K.G., 2014. Microbial succession and the functional potential during the fermentation of Chinese soy sauce brine. Front. Microbiol. 5, 556.
53. Tallapragada, P., Dikshit, R., Jadhav, A., Sarah, U., 2017. Partial purification and characterization of amylase enzyme under solid state fermentation from Monascus sanguineus. J. Genet. Eng. Biotech. 15, 95-101.
54. Tamang, J.P., Watanabe, K., Holzapfel, W.H., 2016. Review: Diversity of microorganisms in global fermented foods and beverages. Front. Microbiol. 7, 377.
55. Tang, J., Tang, X., Tang, M., Zhang, X., Xu, X., Yi, Y., 2017. Analysis of the bacterial communities in two liquors of Soy Sauce aroma as revealed by high-throughput sequencing of the 16S rRNA V4 hypervariable region. Biomed Res. Int. 2017, 1-9.
56. Thanh, V.N., Thuy, N.T., Chi, N.T., Hien, D.D., Ha, B.T., Luong, D.T., Ngoc, P.D., Ty, P.V., 2016. New insight into microbial diversity and functions in traditional Vietnamese alcoholic fermentation. Int. J. Food Microbiol. 232, 15-21.
57. Tseng, Y., Chen, M., Lin, C., 2000. Growth, pigment production and protease activity of Monascus purpureus as affected by salt, sodium nitrite, polyphosphate and various sugars. J. Appl. Microbiol. 88, 31-37.
58. Van Waes, C., Baert, J., Carlier, L., Van Bockstaele, E., 1998. A rapid determination of the total sugar content and the average inulin chain length in roots of chicory (Cichorium intybusL). J. Sci. Food Agr. 76, 107-110.
59. Wan, Y.L., Han, H.X., Li, L., Wu, X.J., Gao, M.X., 2015. Effect of low-frequency magnetic feld on gamma-aminobutyric acid produced by Monascus purpureus in solid-state fermentation. J. Agr. Sci. Tech-Iran.17, 94-98.
60. Wang, Z.M., Lu, Z.M., Shi, J.S., Xu, Z.H., 2016. Exploring flavour-producing core microbiota in multispecies solid-state fermentation of traditional Chinese vinegar. Sci Rep-UK 6, 26818.
61. Wei, C.L., Chao, S.H., Tsai, W.B., Lee, P.S., Tsau, N.H., Chen, J.S., Lai, W.L., Tu, C.Y., Tsai, Y.C., 2013. Analysis of bacterial diversity during the fermentation of inyu, a high-temperature fermented soy sauce, using nested PCR-denaturing gradient gel electrophoresis and the plate count method. Food Microbiol. 33, 252-261.
62. Wu, H., Zhang, S., Ma, Y., Zhou, J., Luo, H., Yang, J., 2017. Comparison of microbial communities in the fermentation starter used to brew Xiaoqu liquor. J. I. Brewing 123, 113-120.
63. Xia, X., Li, G., Zheng, J., Ran, C., Kan, J., 2014. Biochemical, textural and microstructural changes in whole-soya bean cotyledon sufu during fermentation. Int. J. Food Sci. Tech. 49, 1834-1841.
64. Yang, H., Zou, H., Qu, C., Zhang, L., Liu, T., Wu, H., Li, Y., 2014a. Dominant microorganisms during the spontaneous fermentation of Suan Cai, a Chinese fermented vegetable. Food Sci. Technol. Res. 20, 915-926.
65. Yang, J., Ding, X., Qin, Y., Zeng, Y., 2014b. Safety assessment of the biogenic amines in fermented soya beans and fermented bean curd. J. Agr. Food Chem. 62, 7947-7954.
66. Zhang, H.T., HU, Y., HOU, F.L., Zhang, G.J., 2014. Research on the production of low-salt sufu and its physical and chemical properties. China Condiment 39, 78-82.