Journal Home > Volume 11 , Issue 3

Several of the fungal species associated with Fuzhuan brick tea (FBT) are considered as potential probiotics, but few studies have investigated the probiotic properties of these fungi. Here, we isolated 18 fungal strains from two types of FBT and identified these strains based on internal transcribed spacer (ITS) fragment sequence similarity to reference strains (sequence similarity > 98%). Of the 18 strains, 10 tolerated simulated human digestive conditions for sufficient periods in vitro: pH 2-3, 0.3%-0.5% (m/V) bile salts, and artificial gastrointestinal juices. We then measured the antimicrobial activity of the remaining 10 strains against 5 enteropathogenic bacteria and tested the bacteriostatic effects of the thalli and fermentation broth extracts. Of the 6 strains with strong bacteriostatic effects, we eliminated Eurotium cristatum S-9 due to its low hydrophobicity of (26.12 ± 0.35)%. Finally, 2 exhibited good adhesion abilities to human cells (> 100%). Notably, 2 strains can survive in vivo, because they can be isolated from C57BL/6 mice feces. Thus, 2 strains, Aspergillus cristatus H-1 and A. cristatus H-5, are herein identified as promising candidate probiotic strains. It may be put forward a novel research focus on evaluating potential probiotic fungi from FBT.


menu
Abstract
Full text
Outline
About this article

Fungi with potential probiotic properties isolated from Fuzhuan brick tea

Show Author's information Xin Wanga,bYuanyuan Cuia,bChaowei SangaBin WangaYirong YuanaLin Liua,bYahong Yuana,b( )Tianli Yuea,b,c( )
College of Food Science and Engineering, Northwest A&F University, Yangling 712100, China
Laboratory of Quality & Safety Risk Assessment for Agro-products (YangLing), Ministry of Agriculture, Yangling 712100, China
College of Food Science and Technology, Northwest University, Xi'an 710069, China

Abstract

Several of the fungal species associated with Fuzhuan brick tea (FBT) are considered as potential probiotics, but few studies have investigated the probiotic properties of these fungi. Here, we isolated 18 fungal strains from two types of FBT and identified these strains based on internal transcribed spacer (ITS) fragment sequence similarity to reference strains (sequence similarity > 98%). Of the 18 strains, 10 tolerated simulated human digestive conditions for sufficient periods in vitro: pH 2-3, 0.3%-0.5% (m/V) bile salts, and artificial gastrointestinal juices. We then measured the antimicrobial activity of the remaining 10 strains against 5 enteropathogenic bacteria and tested the bacteriostatic effects of the thalli and fermentation broth extracts. Of the 6 strains with strong bacteriostatic effects, we eliminated Eurotium cristatum S-9 due to its low hydrophobicity of (26.12 ± 0.35)%. Finally, 2 exhibited good adhesion abilities to human cells (> 100%). Notably, 2 strains can survive in vivo, because they can be isolated from C57BL/6 mice feces. Thus, 2 strains, Aspergillus cristatus H-1 and A. cristatus H-5, are herein identified as promising candidate probiotic strains. It may be put forward a novel research focus on evaluating potential probiotic fungi from FBT.

Keywords: Fungi, Fuzhuan brick tea, Candidate probiotics, Probiotic properties, Bacteriostatic activity, Adhesion capacity

References(58)

[1]

Z. Liu, L. Gao, J. Huang, et al., Leading progress on genomics, health benefits and utilization of tea resources in China, Nature 566 (2019) S15-S19

[2]

Y. Xiao, K. Zhong, J.R. Bai, et al., Insight into effects of isolated Eurotium cristatum from Pingwu Fuzhuan brick tea on the fermentation process and quality characteristics of Fuzhuan brick tea, J. Sci. Food Agr. 100 (2020) 3598-3607. https://doi.org/10.1002/jsfa.10353

[3]

Y. Lu, Y. He, S. Zhu, et al., New acylglycosides flavones from Fuzhuan brick tea and simulation analysis of their bioactive effects, Int. J. Mol. Sci. 20 (2019) 494. https://doi.org/10.3390/ijms20030494

[4]

G. Chen, M. Wang, M. Xie, et al., Evaluation of chemical property, cytotoxicity and antioxidant activity in vitro and in vivo of polysaccharides from Fuzhuan brick teas, Int. J. Biol. Macromol. 116 (2018) 120-127. https://doi.org/10.1016/j.ijbiomac.2018.04.184

[5]

D. Kang, M. Su, Y. Duan, et al., Eurotium cristatum, a potential probiotic fungus from Fuzhuan brick tea, alleviated obesity in mice by modulating gut microbiota, Food Funct. 10 (2019) 5032-5045. https://doi.org/10.1039/c9fo00604d

[6]

B. Liu, T. Yang, L. Zeng, et al., Crude extract of Fuzhuan brick tea ameliorates DSS-induced colitis in mice, Int. J. Food Sci. Tech. 51 (2016) 2574-2582. https://doi.org/10.1111/ijfs.13241

[7]

T.J. Ling, X.C. Wan, W.W. Ling, et al., New triterpenoids and other constituents from a special microbial-fermented tea-Fuzhuan brick tea, J. Agric. Food Chem. 58 (2010) 4945-4950. https://doi.org/10.1021/jf9043524

[8]

P. Zhao, M. Alam, S.H. Lee, Protection of UVB-induced photoaging by Fuzhuan-brick tea aqueous extract via MAPKs/Nrf2-mediated down-regulation of MMP-1, Nutrients 11 (2018) 60. https://doi.org/10.3390/nu11010060

[9]

D. Liu, J. Huang, Y. Luo, et al., Fuzhuan brick tea attenuates high-fat diet-induced obesity and associated metabolic disorders by shaping gut microbiota, J. Agric. Food Chem. 67 (2019) 13589-13604. https://doi.org/10.1021/acs.jafc.9b05833

[10]

Y. Xiao, K. Zhong, J.R. Bai, et al., The biochemical characteristics of a novel fermented loose tea by Eurotium cristatum (MF800948) and its hypolipidemic activity in a zebrafish model, LWT-Food Sci. Technol. 117 (2020) 108629. https://doi.org/10.1016/j.lwt.2019.108629

[11]

D.M. Lee, M.L. Battson, D.K. Jarrell, et al., Fuzhuan tea reverses arterial stiffening after modest weight gain in mice, Nutrition 33 (2016) 266-270. https://doi.org/10.1016/j.nut.2016.07.010

[12]

Q. Li, J. Huang, Y. Li, et al., Fungal community succession and major components change during manufacturing process of Fu brick tea, Sci. Rep. 7 (2017) 6947. https://doi.org/10.1038/s41598-017-07098-8

[13]

A. Xu, Y. Wang, J. Wen, et al., Fungal community associated with fermentation and storage of Fuzhuan brick-tea, Int. J. Food Microbiol. 146 (2011) 14-22. https://doi.org/10.1016/j.ijfoodmicro.2011.01.024

[14]

Y. Yao, M. Wu, Y. Huang, et al., Appropriately raising fermentation temperature beneficial to the increase of antioxidant activity and gallic acid content in Eurotium cristatum-fermented loose tea, LWT-Food Sci. Technol. 82 (2017) 248-254. https://doi.org/10.1016/j.lwt.2017.04.032

[15]

L.Y. Chan, M. Takahashi, P.J. Lim, et al., Eurotium cristatum fermented okara as a potential food ingredient to combat diabetes, Sci. Rep. 9 (2019) 17536. https://doi.org/10.1038/s41598-019-54021-4

[16]

S.D. Zhou, X. Xu, Y.F. Lin, et al., On-line screening and identification of free radical scavenging compounds in Angelica dahurica fermented with Eurotium cristatum using an HPLC-PDA-Triple-TOF-MS/MS-ABTS system, Food Chem. 272 (2019) 670-678. https://doi.org/10.1016/j.foodchem.2018.07.173

[17]

Q. Gu, G. Duan, X. Yu, Bioconversion of flavonoid glycosides from hippophae rhamnoides leaves into flavonoid aglycones by Eurotium amstelodami, Microorganisms 7 (2019) 122. https://doi.org/10.3390/microorganisms7050122

[18]

S. Takenaka, R. Nakabayashi, C. Ogawa, et al. Characterization of surface Aspergillus community involved in traditional fermentation and ripening of katsuobushi, Int. J. Food Microbiol. 327 (2020) 108654. https://doi.org/10.1016/j.ijfoodmicro.2020.108654

[19]

O.M. Salama, N.M. Fathallah, M.M. Raafat, et al., Bio-guided fractionation of prenylated benzaldehyde derivatives as potent antimicrobial and antibiofilm from Ammi majus L. fruits-associated Aspergillus amstelodami, Planta. Med. 85 (2019) 1473-1474. https://doi.org/10.1055/s-0039-3399859

[20]

K. Waing, J. Gutierrez, C. Galvez, et al., Molecular identification of leaf litter fungi potential for cellulose degradation, Mycosphere 6 (2015) 139-144. https://doi.org/10.5943/mycosphere/6/2/3

[21]

C. Hill, F. Guarner, G. Reid, et al., The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic, Nat. Rev. Gastroenterol. Hepatol. 11 (2014) 506-514. https://doi.org/10.1038/nrgastro.2014.66

[22]

L. Cassani, A. Gomez-Zavaglia, J. Simal-Gandara, Technological strategies ensuring the safe arrival of beneficial microorganisms to the gut: from food processing and storage to their passage through the gastrointestinal tract, Food Res. Int. 129 (2020) 20. https://doi.org/10.1016/j.foodres.2019.108852

[23]

N.K. Lee, J.Y. Hong, S.H. Yi, et al., Bioactive compounds of probiotic Saccharomyces cerevisiae strains isolated from cucumber jangajji, J. Funct. Foods 58 (2019) 324-329. https://doi.org/10.1016/j.jff.2019.04.059

[24]

B.P. Montoro, N. Benomar, N.C. Gomez, et al., Proteomic analysis of Lactobacillus pentosus for the identification of potential markers involved in acid resistance and their influence on other probiotic features, Food Microbiol. 72 (2018) 31-38. https://doi.org/10.1016/j.fm.2017.11.006

[25]

R.A. Samson, C.M. Visagie, J. Houbraken, et al., Phylogeny, identification and nomenclature of the genus Aspergillus, Stud. mycol. 78 (2014) 141-173. https://doi.org/10.1016/j.simyco.2014.07.004

[26]

W.W. May Zin, S. Buttachon, T. Dethoup, et al., Antibacterial and antibiofilm activities of the metabolites isolated from the culture of the mangrove-derived endophytic fungus Eurotium chevalieri KUFA 0006, Phytochemistry 141 (2017) 86-97. https://doi.org/10.1016/j.phytochem.2017.05.015

[27]

J. Wang, Z. Guo, Q. Zhang, et al., Fermentation characteristics and transit tolerance of probiotic Lactobacillus casei Zhang in soymilk and bovine milk during storage, J. Dairy Sci. 92 (2009) 2468-2476. https://doi.org/10.3168/jds.2008-1849

[28]

X. Wang, Y.X. Zhang, T.T. Ren, et al., Isolation and identification of Eurotium cristatum from Fuzhuan tea and its application in liquid-state fermentation, Food Sci. 40 (2019) 172-178. https://doi.org/10.7506/spkx1002-6630-20180820-207

[29]

I. Mantzourani, P. Chondrou, C. Bontsidis, et al., Assessment of the probiotic potential of lactic acid bacteria isolated from kefir grains: evaluation of adhesion and antiproliferative properties in in vitro experimental systems, Ann. Microbiol. 69 (2019) 751-763. https://doi.org/10.1007/s13213-019-01467-6

[30]

C.G. Vinderola, J.A. Reinheimer, Lactic acid starter and probiotic bacteria: a comparative "in vitro" study of probiotic characteristics and biological barrier resistance, Food Res. Int. 36 (2003) 895-904. https://doi.org/10.1016/S0963-9969(03)00098-X

[31]

P.F. De Palencia, P. Lopez, A.L. Corbi, et al., Probiotic strains: survival under simulated gastrointestinal conditions, in vitro adhesion to Caco-2 cells and effect on cytokine secretion, Eur. Food Res. Technol. 227 (2008) 1475-1484. https://doi.org/10.1007/s00217-008-0870-6

[32]

J.T. Bi, P. Ma, Z.W. Yang, et al., Isolation of endophytic fungi from the medicinal plant Tamarix chinensis and their microbial inhibition activity, Acta. Prat. Sin. 22 (2013) 132-138. https://doi.org/10.11686/cyxb20130317

[33]

J. Yang, J. Wang, K. Yang, et al., Antibacterial activity of selenium-enriched lactic acid bacteria against common food-borne pathogens in vitro, J. Dairy Sci. (2017) 1930-1942. https://doi.org/10.3168/jds.2017-13430

[34]

E. Kaczorek, L. Chrzanowski, A. Pijanowska, et al., Yeast and bacteria cell hydrophobicity and hydrocarbon biodegradation in the presence of natural surfactants: rharnnolipides and saponins, Bioresource Technol. 99 (2008) 4285-4291. https://doi.org/10.1016/j.biortech.2007.08.049

[35]

A. Vasiee, S.A. Mortazavi, M. Sankian, et al., Antagonistic activity of recombinant Lactococcus lactis NZ1330 on the adhesion properties of Escherichia coli causing urinary tract infection, Microb. Pathog. 133 (2019) 103547. https://doi.org/10.1016/j.micpath.2019.103547

[36]

C.F. Guo, L.W. Zhang, X. Han, et al., Screening for cholesterol-lowering probiotic based on deoxycholic acid removal pathway and studying its functional mechanisms in vitro, Anaerobe 18 (2012) 516-522. https://doi.org/10.1016/j.anaerobe.2012.08.003

[37]

G. Krausova, I. Hyrslova, I. Hynstova, In vitro evaluation of adhesion capacity, hydrophobicity, and auto-aggregation of newly isolated potential probiotic strains, Fermentation 5 (2019) 100. https://doi.org/10.3390/fermentation5040100

[38]

A. Garcia-Ruiz, D.G. de Llano, A. Esteban-Fernandez, et al., Assessment of probiotic properties in lactic acid bacteria isolated from wine, Food Microbiol. 44 (2014) 220-225. https://doi.org/10.1016/j.fm.2014.06.015

[39]

X. Wang, X.X. Li, B. Liu, et al., Comparison of chemical constituents of Eurotium cristatum-mediated pure and mixed fermentation in summer-autumn tea, LWT–Food Sci. Technol. 143 (2021) 111132. https://doi.org/10.1016/j.lwt.2021.111132

[40]

F.O. Stefani, T.H. Bell, C. Marchand, et al., Culture-dependent and -independent methods capture different microbial community fractions in hydrocarbon-contaminated soils, PLoS One 10 (2015) 6. https://doi.org/10.1371/journal.pone.0128272

[41]

O. Carrion, D. Minanagalbis, M.J. Montes, et al., Pseudomonas deceptionensis sp. nov., a psychrotolerant bacterium from the antarctic, Int. J. Syst. Evol. Micr. 61 (2011) 2401-2405. https://doi.org/10.1099/ijs.0.024919-0

[42]

Y. Rui, P. Wan, G. Chen, et al., Analysis of bacterial and fungal communities by Illumina MiSeq platforms and characterization of Aspergillus cristatus in Fuzhuan brick tea, LWT-Food Sci. Technol. 110 (2019) 168-174. https://doi.org/10.1016/j.lwt.2019.04.092

[43]

M.Y. Li, Y. Xiao, K. Zhong, et al., Study on taste characteristics and microbial communities in Pingwu Fuzhuan brick tea and the correlation between microbiota composition and chemical metabolites, J. Food Sci. Tech. Mys. 6 (2021). https://doi.org/10.1007/s13197-021-04976-y

[44]

C.L. Ramos, L. Thorsen, R.F. Schwan, et al., Strain-specific probiotics properties of Lactobacillus fermentum, Lactobacillus plantarum and Lactobacillus brevis isolates from brazilian food products, Food Microbiol. 36 (2013) 22-29. https://doi.org/10.1016/j.fm.2013.03.010

[45]

L. Morelli, In vitro assessment of probiotic bacteria: from survival to functionality, Int. Dairy J. 17 (2007) 1278-1283. https://doi.org/10.1016/j.idairyj.2007.01.015

[46]

N. Radic, B. Strukelj, Endophytic fungi-the treasure chest of antibacterial substances, Phytomedicine 19 (2012) 1270-1284. https://doi.org/10.1016/j.phymed.2012.09.007

[47]

F. Gaggìa, P. Mattarelli, B. Biavati, Probiotics and prebiotics in animal feeding for safe food production, Int. J. Food Microbiol. 141 (2010) S15-S28. https://doi.org/10.1016//j.ijfoodmicro.2010.02.031

[48]

C.M.S. Ambrosio, S.M. de Alencar, R.L.M. de Sousa, et al., Antimicrobial activity of several essential oils on pathogenic and beneficial bacteria, Ind. Crop. Prod. 97 (2017) 128-136. https://doi.org/10.1016/j.indcrop.2016.11.045

[49]

C. Xu, J.L. Li, L.Q. Yang, et al., Antibacterial activity and a membrane damage mechanism of Lachnum YM30 melanin against Vibrio parahaemolyticus and Staphylococcus aureus, Food Control 73 (2017) 1445-1451. https://doi.org/10.1016/j.foodcont.2016.10.048

[50]

F.Y. Du, X.M. Li, C.S. Li, et al., Cristatumins A–D, new indole alkaloids from the marine-derived endophytic fungus Eurotium cristatum EN-220, Bioorg. Med. Chem. Lett. 22 (2012) 4650-4653. https://doi.org/10.1016/j.bmcl.2012.05.088

[51]

P. Zhang, C. Jia, Y. Deng, et al., Anti-inflammatory prenylbenzaldehyde derivatives isolated from Eurotium cristatum, Phytochemistry 158 (2019). 120-125. https://doi.org/10.1016/j.phytochem.2018.11.017

[52]

J.T. Smith, J.M. Hamilton-Miller, Differences between pencillinases from gram-positive and gram-negative bacteria, Nature 197 (1963) 976-978. https://doi.org/10.1038/197976a0

[53]

R. Vij, C. Danchik, C. Crawford, et al., Variation in cell surface hydrophobicity among Cryptococcus neoformans strains influences interactions with amoebas, mSphere 5 (2020) 2. https://doi.org/10.1128/mSphere.00310-20

[54]

A. Kourelis, C. Kotzamanidis, E. Litopoulou-Tzanetaki, et al., Determination of in vitro probiotic properties of yeast strains isolated from feta cheese and infants, J. Biol. Res. 13 (2010) 93-104

[55]

A. Krasowska, K. Sigler, How microorganisms use hydrophobicity and what does this mean for human needs, Front. Cell. Infect. Microbiol. 4 (2014) 112. https://doi.org/10.3389/fcimb.2014.00112

[56]

L. Meng, S. Zhou, X. Xu, et al., A multi-scale approach to investigate adhesion properties of Pseudomonas aeruginosa PAO1 to geotrichum candidum LG-8, a potential probiotic yeast, Foods 9 (2020) 7. https://doi.org/10.3390/foods9070912

[57]

J.S. Liu, D.G. Hu, Y.Q. Chen, et al., Strain-specific properties of Lactobacillus plantarum for prevention of Salmonella infection, Food Funct. 9 (2018) 3673-3682. https://doi.org/10.1039/c8fo00365c

[58]

B. Aktas, T.J. De Wolfe, N. Safdar, et al., The impact of Lactobacillus casei on the composition of the cecal microbiota and innate immune system is strain specific, PLoS One 11 (2016) 15. https://doi.org/10.1371/journal.pone.0156374

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 18 May 2021
Revised: 01 September 2021
Accepted: 05 September 2021
Published: 04 February 2022
Issue date: May 2022

Copyright

© 2022 Beijing Academy of Food Sciences.

Acknowledgements

This research was supported by the Shaanxi Special Project of China (2018ZDXM-NY-084).

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return