Skip to main content
Log in

In Vitro Evaluation of Probiotic Potential of Lactic Acid Bacteria Isolated from Yunnan De’ang Pickled Tea

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

This study aimed to investigate the probiotic potential of lactic acid bacteria (LAB) strains isolated from De’ang pickled tea, a traditional food consumed by the De’ang nationality of Yunnan, China. Twenty-six LAB strains isolated from De’ang pickled tea were subjected to identification based on 16S rRNA gene sequence analysis. Twenty-four belonged to Lactobacillus plantarum, one belonged to Enterococcus casseliflavus, and one belonged to Lactobacillus acidophilus. Eighteen out of 26 LAB strains which showed a higher capability to tolerate simulated gastrointestinal juices were chosen to further evaluate their probiotic properties. Varied adhesive abilities and auto-aggregative capacities of selected LAB strains were dependent on species and even strains. All tested LAB strains were resistant to kanamycin, streptomycin, gentamycin, and vancomycin and sensitive to tetracycline and chloramphenicol. Ten out of the 18 strains are resistant to ampicillin, and the remaining strains are sensitive to ampicillin; 4 out of the 18 strains showed resistance to erythromycin. Compared to reference strain Lactobacillus rhamnosus strain GG, these LAB strains had a greater or comparative antimicrobial activity against Salmonella typhimurium or Escherichia coli. In contrast, eight out of the 18 strains suppressed growth of Shigella flexneri. Two L. plantarum strains, ST and STDA10, not only exhibited good probiotic properties but also showed a good ability of scavenging DPPH and ABTS+. This study suggests that L. plantarum ST and STDA10 could be used as potential probiotics applied in functional foods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Wang D, Lu J, Miao A, Xie Z, Yang D (2008) HPLC-DAD-ESI-MS/MS analysis of polyphenols and purine alkaloids in leaves of 22 tea cultivars in China. J Food Compos Anal 21(5):361–369. https://doi.org/10.1016/j.jfca.2008.01.002

    Article  CAS  Google Scholar 

  2. Gong Z, Watanabe N, Yagi A, Etoh H, Sakata K, Ina K, Liu Q (1993) Compositional change of pu-erh tea during processing. Biosci Biotech Bioch 57:1745–1746

    Article  CAS  Google Scholar 

  3. Nanba A, Miyagawa K, Omori M, Kato M, Tamura A, Saito H (1998) Non-salted pickled tea (sour tea) in south-east Yunnan in China. Japan Soc Home Econ 49:907–915

    Google Scholar 

  4. Han T, Aye KN (2015) The legend of laphet: a Myanmar fermented tea leaf. J Ethn Foods 2(4):173–178. https://doi.org/10.1016/j.jef.2015.11.003

    Article  Google Scholar 

  5. Hiasa M, Kurokawa M, Ohta K, Esumi T, Akita H, Niki K, Yagi Y, Echigo N, Hatakeyama D, Kuzuhara T (2013) Identification and purification of resorcinol, an antioxidant specific to Awa-ban (pickled and anaerobically fermented) tea. Food Res Int 54(1):72–80. https://doi.org/10.1016/j.foodres.2013.05.036

    Article  CAS  Google Scholar 

  6. Kanpiengjai A, Chui-Chai N, Chaikaew S, 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 5:121–131

    Article  Google Scholar 

  7. Tanasupawat S, Pakdeeto A, Thawai C, Yukphan P, Okada S (2007) Identification of lactic acid bacteria from fermented tea leaves (miang) in Thailand and proposals of Lactobacillus thailandensis sp. nov., Lactobacillus camelliae sp. nov., and Pediococcuss iamensis sp. nov. J Gen Appl Microbiol 53(1):7–15. https://doi.org/10.2323/jgam.53.7

    Article  CAS  PubMed  Google Scholar 

  8. Xiao P, Huang Y, W1 Y, B1 Z, Quan X (2015) Screening lactic acid bacteria with high yielding-acid capacity from pickled tea for their potential uses of inoculating to ferment tea products. J Food Sci Tech 52(10):6727–6734. https://doi.org/10.1007/s13197-015-1803-6

  9. FAO/WHO (2006) Probiotics in food: health and nutritional properties and guidelines for evaluation. Rome, p 85

  10. Argyri AA, Zoumpopoulou G, Karatzas KA, Tsakalidou E, Nychas GJ, Panagou EZ, Tassou CC (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33(2):282–291. https://doi.org/10.1016/j.fm.2012.10.005

    Article  CAS  PubMed  Google Scholar 

  11. Leatherhead Food International (2006) The international market for functional foods. 3rd ed., Functional food market report (ISBN 1 904007-82-1)

  12. García-Ruiz A, González de Llano D, Esteban-Fernández A, Requena T, Bartolomé B, Moreno-Arribas MV (2014) Assessment of probiotic properties in lactic acid bacteria isolated from wine. Food Microbiol l44:220–225

    Article  Google Scholar 

  13. Peres CM, Peres C, Hernández-Mendoza A, Malcata FX (2012) Review on fermented plant materials as carriers and sources of potentially probiotic lactic acid bacteria—with an emphasis on table olives. Trends Food Sci Tech 26(1):31–42. https://doi.org/10.1016/j.tifs.2012.01.006

    Article  CAS  Google Scholar 

  14. Karasu N, Şimşek Ö, Çon AH (2010) Technological and probiotic characteristics of Lactobacillus plantarum strains isolated from traditionally produced fermented vegetables. Ann Microbiol 60(2):227–234. https://doi.org/10.1007/s13213-010-0031-6

    Article  CAS  Google Scholar 

  15. Cao ZH, Pan HB, Tian RJ, Rong H, Gu DH, Jia JJ, Ge CR, Lin QY (2016) In vitro evaluation of probiotic potential of Pediococcus pentosaceus L1 isolated from paocai, a Chinese fermented vegetable. Ann Microbiol 66(3):963–971. https://doi.org/10.1007/s13213-015-1182-2

    Article  CAS  Google Scholar 

  16. Zhang Y, Zhang L, Du M, Yi H, Guo C, Tuo Y, Han X, Li J, Zhang L, Yang L (2011) Antimicrobial activity against Shigella sonnei and probiotic properties of wild lactobacilli from fermented food. Microbiol Res 167:27–31

    Article  PubMed  Google Scholar 

  17. Kos B, Susković J, Vuković S, Simpraga M, Frece J, Matosić S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94(6):981–987. https://doi.org/10.1046/j.1365-2672.2003.01915.x

    Article  CAS  PubMed  Google Scholar 

  18. Ilavenil S, Vijayakumar M, Kim DH, Valan Arasu M, Park HS, Ravikumar S, Choi KC (2015) Assessment of probiotic, antifungal and cholesterol lowering properties of Pediococcus pentosaceus KCC-23 isolated from Italian ryegrass. J Sci Food Agric doi 96(2):593–601. https://doi.org/10.1002/jsfa.7128

    Article  CAS  Google Scholar 

  19. Franklin RC, Matthew AW, Jeff A, Michael ND, George ME (2012) Performance standards for antimicrobial susceptibility testing. Twenty-second informational supplement. Clinical and laboratory standards institute (CLSI): Wayne, PA, USA

  20. Tejero-Sariñena S, Barlow J, Costabile A, Gibson GR, Rowland I (2012) In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. Anaerobe 18(5):530–538. https://doi.org/10.1016/j.anaerobe.2012.08.004

    Article  CAS  PubMed  Google Scholar 

  21. Jin D, Chen C, Li L, Lu S, Li Z, Zhou Z, Jing H, Xu Y, Du P, Wang H, Xiong Y, Zheng H, Bai X, Sun H, Wang L, Ye C, Gottschalk M, Xu J (2013) Dynamics of fecal microbial communities in children with diarrhea of unknown etiology and genomic analysis of associated Streptococcus lutetiensis. BMC Microbiol 13(1):141. https://doi.org/10.1186/1471-2180-13-141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ammor MS, Flórez AB, Mayo B (2007) Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol 24(6):559–570. https://doi.org/10.1016/j.fm.2006.11.001

    Article  CAS  PubMed  Google Scholar 

  23. Di Cagno R, Coda R, De Angelis M, Gobbetti M (2013) Exploitation of vegetables and fruits through lactic acid fermentation. Food Microbiol 33(1):1–10. https://doi.org/10.1016/j.fm.2012.09.003

    Article  CAS  PubMed  Google Scholar 

  24. Rodríguez H, Curiel JA, Landete JM, de las Rivas B, López de Felipe F, Gómez-Cordovés C, Mancheño JM, Muñoz R (2009) Food phenolics and lactic acid bacteria. Int J Food Microbiol 132(2-3):79–90. https://doi.org/10.1016/j.ijfoodmicro.2009.03.025

    Article  CAS  PubMed  Google Scholar 

  25. Ankolekar C, Johnson D, Pinto Mda S, Johnson K, Labbe R, Shetty K (2011) Inhibitory potential of tea polyphenolics and influence of extraction time against Helicobacter pylori and lack of inhibition of beneficial lactic acid bacteria. J Med Food 14(11):1321–1329. https://doi.org/10.1089/jmf.2010.0237

    Article  CAS  PubMed  Google Scholar 

  26. Zhao D, Shah NP (2016) Lactic acid bacterial fermentation modified phenolic composition in tea extracts and enhanced their antioxidant activity and cellular uptake of phenolic compounds following in vitro digestion. J Funct Foods 20:182–194. https://doi.org/10.1016/j.jff.2015.10.033

    Article  CAS  Google Scholar 

  27. Lee H, Yoon H, Ji Y, Kim H, Park H, Lee J, Shin H, Holzapfel W (2011) Functional properties of Lactobacillus strains isolated from kimchi. Int J Food Microbiol 145(1):155–161. https://doi.org/10.1016/j.ijfoodmicro.2010.12.003

    Article  CAS  PubMed  Google Scholar 

  28. Vitali B, Minervini G, Rizzello CG, Spisni E, Maccaferri S, Brigidi P, Gobbetti M, Di Cagno R (2012) Novel probiotic candidates for humans isolated from raw fruits and vegetables. Food Microbiol 31(1):116–125. https://doi.org/10.1016/j.fm.2011.12.027

    Article  CAS  PubMed  Google Scholar 

  29. Huang R, Tao X, Wan C, Li S, Xu H, Xu F, Shah NP, Wei H (2015) In vitro probiotic characteristics of Lactobacillus plantarum ZDY 2013 and its modulatory effect on gut microbiota of mice. J Dairy Sci 98(9):5850–5861. https://doi.org/10.3168/jds.2014-9153

    Article  CAS  PubMed  Google Scholar 

  30. Breidt F, McFeeters RF, Díaz-Muñiz I (2007) Fermented vegetables. In: Doyle PD, Beuchat LR (eds) Food microbiology: fundamentals and frontiers, third edition. ASM Press, Washington, DC, pp 783–784. https://doi.org/10.1128/9781555815912.ch36

    Chapter  Google Scholar 

  31. Kleerebezem M, Hols P, Bernard E, Rolain T, Zhou M, Siezen RJ, Bron PA (2010) The extracellular biology of the lactobacilli. FEMS Microbiol Rev 34(2):199–230. https://doi.org/10.1111/j.1574-6976.2009.00208.x

    Article  CAS  PubMed  Google Scholar 

  32. Lee N, Kim S, Han KJ, Eom SJ, Paik H (2014) Probiotic potential of Lactobacillus strains with anti-allergic effects from kimchi for yogurt starters. LWT - Food Sci Tech 58(1):130–134. https://doi.org/10.1016/j.lwt.2014.02.028

    Article  CAS  Google Scholar 

  33. Oguntoyinbo FA, Narbad A (2015) Multifunctional properties of Lactobacillus plantarum strains isolated from fermented cereal foods. J Funct Foods 17:621–631. https://doi.org/10.1016/j.jff.2015.06.022

    Article  CAS  Google Scholar 

  34. Felten A, Barreau C, Bizet C, Lagrange PH, Philippon A (1999) Lactobacillus species identification, H2O2 production, and antibiotic resistance and correlation with human clinical status. J Clin Microbiol 37(3):729–733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Danielsen M, Wind A (2003) Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol 82:1–11

    Article  CAS  PubMed  Google Scholar 

  36. Liu C, Zhang ZY, Dong K, Yuan JP, Guo XK (2009) Antibiotic resistance of probiotic strains of lactic acid bacteria isolated from marketed foods and drugs. Biomed Environ Sci 22(5):401–412. https://doi.org/10.1016/S0895-3988(10)60018-9

    Article  CAS  PubMed  Google Scholar 

  37. Morrow LE, Gogineni V, Malesker MA (2012) Probiotic, prebiotic, and synbiotic use in critically ill patients. Curr Opin Crit Care 18(2):186–191. https://doi.org/10.1097/MCC.0b013e3283514b17

    Article  PubMed  Google Scholar 

  38. da Silva Sabo S, Vitolo M, González GMD, de Souza Oliveira RP (2014) Overview of Lactobacillus plantarum as a promising bacteriocin producer among lactic acid bacteria. Food Res Int 64:527–536. https://doi.org/10.1016/j.foodres.2014.07.041

    Article  CAS  PubMed  Google Scholar 

  39. Todorov SD, Dicks LMT (2005) Lactobacillus plantarum isolated from molasses produces bacteriocins active against Gram-negative bacteria. Enzyme Microb Tech 36(2-3):318–326. https://doi.org/10.1016/j.enzmictec.2004.09.009

    Article  CAS  Google Scholar 

  40. Kullisar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 72(3):215–224. https://doi.org/10.1016/S0168-1605(01)00674-2

    Article  Google Scholar 

  41. Li S, Zhao Y, Zhang L, Zhang X, Huang L, Li D, Niu C, Yang Z, Wang Q (2012) Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chem 135(3):1914–1919. https://doi.org/10.1016/j.foodchem.2012.06.048

    Article  CAS  PubMed  Google Scholar 

  42. Das D, Goyal A (2015) Antioxidant activity and γ-aminobutyric acid (GABA) producing ability of probiotic Lactobacillus plantarum DM5 isolated from Marcha of Sikkim. LWT-Food Sci Techno l61:263–268

    Article  Google Scholar 

  43. Lin MY, Yen CL (1999) Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47(4):1460–1466. https://doi.org/10.1021/jf981149l

    Article  CAS  PubMed  Google Scholar 

  44. Shen Q, Shang N, Li P (2011) In vitro and in vivo antioxidant activity of Bifidobacterium animalis 01 isolated from centenarians. Curr Microbiol 62(4):1097–1103. https://doi.org/10.1007/s00284-010-9827-7

    Article  CAS  PubMed  Google Scholar 

  45. Xing J, Wang G, Zhang Q, Liu X, Gu Z, Zhang H, Chen YQ, Chen W (2015) Determining antioxidant activities of lactobacilli cell-free supernatants by cellular antioxidant assay: a comparison with traditional methods. PLoS One 10:e0119058

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation of China (Grant No. 31501496 and 31760448) and Applied Basic Research Projects of Yunnan Province (Grant No. 2017FB064).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Qiuye Lin or Zhiyong Zhao.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic Supplementary Material

ESM 1

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cao, Z., Pan, H., Li, S. et al. In Vitro Evaluation of Probiotic Potential of Lactic Acid Bacteria Isolated from Yunnan De’ang Pickled Tea. Probiotics & Antimicro. Prot. 11, 103–112 (2019). https://doi.org/10.1007/s12602-018-9395-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-018-9395-x

Keywords

Navigation