Biochemical components associated with microbial community shift during the pile-fermentation of primary dark tea

Frontiers in Microbiology

Volumn 9, Issue JUL, 2018, Pages

  Li, Qin ^a   Chai, Shuo ^a   Li, Yongdi ^a   Huang, Jianan ^a   Luo, Yu ^b   Xiao, Lizheng ^a   Liu, Zhonghua ^a  

^a HUNAN AGRICULTURAL UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Biochemical components; Food fermentation; Illumina MiSeq sequencing; Microbial community; Primary dark tea

Indexed keywords

AMINO ACID; CELLULASE; CHEMICAL COMPOUND; POLYGALACTURONASE; POLYPHENOL;

ARTICLE; ASPERGILLUS; CYBERLINDNERA; DNA EXTRACTION; DNA SEQUENCE; ECOSYSTEM; ENZYME ANALYSIS; EUROTIUM; FERMENTATION; INFORMATION PROCESSING; KLEBSIELLA; LACTOBACILLUS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; PLANT LEAF; TEA;

EID: 85049863371     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2018.01509     Document Type: Article

References (59)

1. Abe, M., Takaoka, N., Idemoto, Y., Takagi, C., Imai, T., and Nakasaki, K. (2008). Characteristic fungi observed in the fermentation process for Puer tea. Int. J. Food Microbiol. 124, 199-203. doi: 10.1016/j.ijfoodmicro.2008.03.008
2. Ainsworth, G. C. (2014). Ainsworth & Bisby's Dictionary of the Fungi, Vol. 4, 43, 2013. IMA Fungus 5. Wallingford: CAB International
3. Amann, R., and Ludwig, W. (2000). Ribosomal RNA-targeted nucleic acid probes for studies in microbial ecology. FEMS Microbiol. Rev. 24, 555-565. doi: 10.1111/j.1574-6976.2000.tb00557.x
4. Bekatorou, A., Psarianos, C., and Koutinas, A. A. (2006). Production of food grade yeasts. Food Technol. Biotech. 44, 407-415
5. Biz, A., Farias, F. C., Motter, F. A., de Paula, D. H., Richard, P., Krieger, N., et al. (2014). Pectinase activity determination: an early deceleration in the release of reducing sugars throws a spanner in the works! PLoS One 9:e109529. doi: 10.1371/journal.pone.0109529
6. Botella, C., Díaz, A., Ory, I., Webb, C., and Blandino, A. (2007). Xylanase and pectinase production by Aspergillus awamori on grape pomace in solid state fermentation. Process Biochem. 42, 98-101. doi: 10.1016/j.procbio.2006.06.025
7. Bourdichon, F., Casaregola, S., Farrokh, C., Frisvad, J. C., Gerds, M. L., Hammes, W. P., et al. (2012). Food fermentations: microorganisms with technological beneficial use. Int. J. Food Microbiol. 154, 87-97. doi: 10.1016/j.ijfoodmicro.2011.12.030
8. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335. doi: 10.1038/nmeth.f.303
9. Chang, C. F., Liu, Y. R., Chen, S. F., Naumov, G. I., Naumova, E. S., and Lee, C. F. (2012). Five novel species of the anamorphic genus Candida in the Cyberlindnera clade isolated from natural substrates in Taiwan. Antonie Van Leeuwenhoek 102, 9-21. doi: 10.1007/s10482-012-9708-0
10. Cho, J. H., Rathnasingh, C., Song, H., Chung, B. W., Lee, H. J., and Seung, D. (2012). Fermentation and evaluation of Klebsiella pneumoniae and K. oxytoca on the production of 2,3-butanediol. Bioprocess Biosyst. Eng. 35, 1081-1088. doi: 10.1007/s00449-012-0691-697
11. Crous, P. W., Wingfield, M. J., Mansilla, J. P., Alfenas, A. C., and Groenewald, J. Z. (2006). Phylogenetic reassessment of Mycosphaerella spp. and their anamorphs occurring on Eucalyptus. II. Stud. Mycol. 55 (Suppl. C), 99-131. doi: 10.3114/sim.55.1.99
12. Deng, Y., Jiang, Y. H., Yang, Y., He, Z., Luo, F., and Zhou, J. (2012). Molecular ecological network analyses. BMC Bioinformatics 13, 113-113. doi: 10.1186/1471-2105-13-113
13. Du, C., Yan, H., Zhang, Y., Li, Y., and Cao, Z. (2006). Use of oxidoreduction potential as an indicator to regulate 1,3-propanediol fermentation by Klebsiella pneumoniae. Appl. Microbiol. Biotechnol. 69, 554-563. doi: 10.1007/s00253-005-0001-2
14. Du, F. Y., Li, X., Li, X. M., Zhu, L. W., and Wang, B. G. (2017). Indolediketopiperazine alkaloids from Eurotium cristatum EN-220, an endophytic fungus isolated from the marine alga Sargassum thunbergii. Mar. Drugs 15, 1-10. doi: 10.3390/md15020024
15. Du, F. Y., Li, X. M., Li, C. S., Shang, Z., and Wang, B. G. (2012). Cristatumins A-D, new indole alkaloids from the marine-derived endophytic fungus Eurotium cristatum EN-220. Bioorg. Med. Chem. Lett. 22, 4650-4653. doi: 10.1016/j.bmcl.2012.05.088
16. DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., and Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350-356. doi: 10.1021/ac60111a017
17. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200. doi: 10.1093/bioinformatics/btr381
18. Fan, W., Tang, Y., Qu, Y., Cao, F., and Huo, G. (2014). Infant formula supplemented with low protein and high carbohydrate alters the intestinal microbiota in neonatal SD rats. BMC Microbiol. 14:279. doi: 10.1186/s12866-014-0279-2
19. Fu, J., Lv, H., and Chen, F. (2016). Diversity and variation of bacterial community revealed by MiSeq sequencing in chinese dark teas. PLoS One 11:e0162719. doi: 10.1371/journal.pone.0162719
20. Ge, Y., Wang, Y., Liu, Y., Tan, Y., Ren, X., Zhang, X., et al. (2016). Comparative genomic and transcriptomic analyses of the Fuzhuan brick tea-fermentation fungus Aspergillus cristatus. BMC Genomics 17:428. doi: 10.1186/s12864-016-2637-y
21. Harayama, F., and Yasuhira, H. (1994). Miso fermentation using white mutants derived from Aspergillus sojae. J. Brew. Soc. Jpn 89, 901-905. doi: 10.6013/jbrewsocjapan1988.89.901
22. Huang, Y. (1997). Experimental Technique in Tea Sience. Beijing: China Agricultural Press
23. Kamat, S., Gaikwad, S., Ravi Kumar, A., and Gade, W. N. (2013). Xylitol production by Cyberlindnera (Williopsis) saturnus, a tropical mangrove yeast from xylose and corn cob hydrolysate. J. Appl. Microbiol. 115, 1357-1367. doi: 10.1111/jam.12327
24. Kanpiengjai, A., Chui-Chai, N., Chaikaew, S., and Khanongnuch, C. (2016). Distribution of tannin-'tolerant yeasts isolated from Miang, a traditional fermented tea leaf (Camellia sinensis var. assamica) in northern Thailand. Int. J. Food Microbiol. 238, 121-131. doi: 10.1016/j.ijfoodmicro.2016.08.044
25. Li, Q., Huang, J., Li, Y., Zhang, Y., Luo, Y., Chen, Y., et al. (2017). Fungal community succession and major components change during manufacturing process of Fu brick tea. Sci. Rep. 7:6947. doi: 10.1038/s41598-017-07098-8
26. Li, Q., Liu, Z. H., Huang, J. A., Luo, G., Liang, Q. L., Wang, D., et al. (2013). Anti-obesity and hypolipidemic effects of Fuzhuan brick tea water extract in high-fat diet-induced obese rats. J. Sci. Food Agric. 93, 1310-1316. doi: 10.1002/jsfa.5887
27. Li, X. R., Ma, E. B., Yan, L. Z., Meng, H., Du, X. W., Zhang, S. W., et al. (2011). Bacterial and fungal diversity in the traditional Chinese liquor fermentation process. Int. J. Food Microbiol. 146, 31-37. doi: 10.1016/j.ijfoodmicro.2011.01.030
28. Liu, S. Q., and Tsao, M. (2009). Inhibition of spoilage yeasts in cheese by killer yeast Williopsis saturnus var. saturnus. Int. J. Food Microbiol. 131, 280-282. doi: 10.1016/j.ijfoodmicro.2009.03.009
29. Liu, Z. H., Huang, J. A., and Shi, Z. P. (1991). Dynamics of the major enzymes during the primary processing of dark green tea. J. Tea Sci. 11 (Suppl. 1), 17-22
30. Liu, Z. H., Xiao, L. Z., Li, W. S., Chen, H. Q., Zeng, X. J., Xiao, W. J., et al. (2011). The Technique Specification for Raw Anhua Dark Tea Processing. Changsha: Administration of Quality and Technology Supervision of Hunan Province Press
31. Manabe, M. (2001). Fermented foods and mycotoxins. JSM Mycotoxins 51, 25-29. doi: 10.2520/myco.51.25
32. Mukherjee, P. K., Chandra, J., Retuerto, M., Sikaroodi, M., Brown, R. E., Jurevic, R., et al. (2014). Oral mycobiome analysis of HIV-infected patients: identification of Pichia as an antagonist of opportunistic fungi. PLoS Pathog. 10:e1003996. doi: 10.1371/journal.ppat.1003996
33. Newman, M. E. J. (2006). Modularity and community structure in networks. Proc. Natl. Acad. Sci. U.S.A. 103, 8577-8582. doi: 10.1073/pnas.0601602103
34. Norvell, L. L. (2011). Melbourne approves a new code. Mycotaxon 116, 481-490. doi: 10.5248/116.481
35. Pinrou, L., Yuenling, O., Yu, B., Curran, P., and Liu, S. Q. (2010). Evolution of volatile compounds in papaya wine fermented with three Williopsis saturnus yeasts. Int. J. Food Sci. Tech. 45, 2032-2041. doi: 10.1111/j.1365-2621.2010.02369.x
36. Puerari, C., Magalhães-Guedes, K. T., and Schwan, R. F. (2015). Physicochemical and microbiological characterization of chicha, a rice-based fermented beverage produced by Umutina Brazilian Amerindians. Food Microbiol. 46, 210-217. doi: 10.1016/j.fm.2014.08.009
37. Qin, H., Sun, Q., Pan, X., Qiao, Z., and Yang, H. (2016). Microbial diversity and biochemical analysis of Suanzhou: a traditional Chinese fermented cereal Gruel. Front. Microbiol. 7:1311. doi: 10.3389/fmicb.2016.01311
38. Samson, R. A., Visagie, C. M., Houbraken, J., Hong, S. B., Hubka, V., Klaassen, C. H. W., et al. (2014). Phylogeny, identification and nomenclature of the genus Aspergillus. Stud. Mycol. 78, 141-173. doi: 10.1016/j.simyco.2014.07.004
39. Satyanarayana, T., and Kunze, G. (2009). Yeast Biotechnology: Diversity and Applications. Dordrecht: Springer. doi: 10.1007/978-1-4020-8292-4
40. Schloss, P. D., Gevers, D., and Westcott, S. L. (2011). Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310. doi: 10.1371/journal.pone.0027310
41. Takaya, Y., Furukawa, T., Miura, S., Akutagawa, T., Hotta, Y., Ishikawa, N., et al. (2007). Antioxidant constituents in distillation residue of Awamori spirits. J. Agric. Food Chem. 55, 75-79. doi: 10.1021/jf062029d
42. Teng, J., Gong, Z. H., Deng, Y. L., Chen, L., Li, Q., Shao, Y. Y., et al. (2017). Purification, characterization and enzymatic synthesis of theaflavins of polyphenol oxidase isozymes from tea leaf (Camellia sinensis). LWT Food Sci. Technol. 84 (Suppl. C), 263-270. doi: 10.1016/j.lwt.2017.05.065
43. Wang, Z. M., Lu, Z. M., Shi, J. S., and Xu, Z. H. (2016). Exploring flavour-producing core microbiota in multispecies solid-state fermentation of traditional Chinese vinegar. Sci. Rep. 6:26818. doi: 10.1038/srep26818
44. Wang, Z., Shi, Z., Liu, Z., Huang, J., Wen, Q., and Zhu, S. (1991a). Discussion on the mechanism of quality and flavour formation of dark green tea. J. Tea Sci. 11(Suppl. 1), 1-9
45. Wang, Z., Tan, H., and Shi, L. (1991b). Dynamics of major nitrogenous compounds during the promary processing of dark green tea. J. Tea Sci. 11(Suppl. 1), 29-33
46. Wang, Z., Zhang, Y., Tong, X., and Liu, Z. (1991c). Dynamics of polyphenols and carbohydrates during the primary processing of dark green tea. J. Tea Sci. 11(Suppl. 1), 23-28
47. Ward, O. P., Qin, W. M., Dhanjoon, J., Ye, J., and Singh, A. (2005). "Physiology and biotechnology of Aspergillus," in Advances in Applied Microbiology, eds J. W. B. G. M. G. Allen, I. Laskin, and S. Sima Cambridge: Academic Press), 1-75
48. Wen, Q. Y., and Liu, S. C. (1991). Variation of the microorganism groups during the pile-fermentation of dark green tea. J. Tea Sci. 11(Suppl. 1), 10-16
49. Wicklow, D. T., McAlpin, C. E., and Yeoh, Q. L. (2007). Diversity of Aspergillus oryzae genotypes (RFLP) isolated from traditional soy sauce production within Malaysia and Southeast Asia. Mycoscience 48, 373-380. doi: 10.1007/s10267-007-0383-3
50. Wood, T. M., and Bhat, K. M. (1988). Methods for measuring cellulase activities. Methods Enzymol. 160, 87-112. doi: 10.1016/0076-6879(88)60109-1
51. Xiong, J., Liu, Y., Lin, X., Zhang, H., Zeng, J., Hou, J., et al. (2012). Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ. Microbiol. 14, 2457-2466. doi: 10.1111/j.1462-2920.2012.02799.x
52. Xu, A., Wang, Y., Wen, J., Liu, P., Liu, Z., and Li, Z. (2011). Fungal community associated with fermentation and storage of Fuzhuan brick-tea. Int. J. Food Microbiol. 146, 14-22. doi: 10.1016/j.ijfoodmicro.2011.01.024
53. Xu, J. F., Zhou, W. L., Lu, X. L., Wang, J., and Sha, H. T. (2013). Tea-Determination of Free Amino Acids Content. Beijing: Standardization Administration of The People's Republic of China Press
54. Yang, Y., Deng, Y., Jin, Y., Liu, Y., Xia, B., and Sun, Q. (2017). Dynamics of microbial community during the extremely long-term fermentation process of a traditional soy sauce. J. Sci. Food Agric. 97, 3220-3227. doi: 10.1002/jsfa.8169
55. Zhang, L., Zhang, Z., Zhou, Y., Ling, T., and Wan, X. (2013). Chinese dark teas: postfermentation, chemistry and biological activities. Food Res. Int. 53, 600-607. doi: 10.1016/j.foodres.2013.01.016
56. Zhao, M., Xiao, W., Ma, Y., Sun, T., Yuan, W., Tang, N., et al. (2013). Structure and dynamics of the bacterial communities in fermentation of the traditional Chinese post-fermented pu-erh tea revealed by 16S rRNA gene clone library. World J. Microbiol. Biotechnol. 29, 1877-1884. doi: 10.1007/s11274-013-1351-z
57. Zhao, M., Zhang, D. L., Su, X. Q., Duan, S. M., Wan, J. Q., Yuan, W. X., et al. (2015). An integrated metagenomics/metaproteomics investigation of the microbial communities and enzymes in solid-state fermentation of Pu-erh tea. Sci. Rep. 5:10117. doi: 10.1038/srep10117
58. Zhou, W. L., Xu, J. F., Lu, X. L., Wang, J., and Sha, H. T. (2013). Tea-Determination of Water Extract Content. Beijing: Standardization Administration of The People's Republic of China Press
59. Zou, X., Li, Y., Zhang, X., Li, Q., Liu, X., Huang, Y., et al. (2014). A new prenylated indole diketopiperazine alkaloid from Eurotium cristatum. Molecules 19, 17839-17847. doi: 10.3390/molecules191117839