Probiotic properties of Lactobacillus strains with high cinnamoyl esterase activity isolated from jeot-gal, a high-salt fermented seafood

  • Jong-Hui Kim
  • Sang-Ho BaikEmail author
Original Article


Cinnamoyl esterases (CEs) improve the bioavailability of caffeic acid, a potent antioxidant with beneficial health effects. This study aimed to characterize the probiotic properties of 14 strains of CE-producing lactic acid bacteria (LAB) isolated from jeot-gal, a high-salt fermented seafood. We evaluated properties of the probiotic LAB with high CE activity, including tolerance to low pH and bile salts, antimicrobial activity, surface hydrophobicity, adhesion, and immunomodulatory effects, in vitro. All LAB tested tolerated pH 2.0 and 3% Oxgall, i.e., conditions comparable with those in the gastrointestinal environment. Three isolates, Lactobacillus paracasei JBCC10650, Lactobacillus pentosus JBCC10659, and Lactobacillus plantarum JBCC10543, showed stronger adherence to epithelial cells (12.3, 9.6, and 9.4%) than a commercial probiotic Lactobacillus rhamnosus GG (9.1%; p < 0.05), and exhibited broad antibacterial activity against putative pathogens. Most of the 14 LAB strains were able to regulate mRNA expression of pro- and anti-inflammatory cytokines in macrophages, indicating their potential immunomodulatory effects. Our findings suggest that the newly isolated CE-producing probiotics may show beneficial health effects by supporting the host immune system.


Adhesion Cinnamoyl esterase Cytokine Lactobacillus Probiotics 



Caffeic acid


Cinnamoyl esterase


Chlorogenic acid


Lactic acid bacteria


Funding information

This research was supported by the Ministry of Trade, Industry & Energy (MOTIE), Korea Institute for Advancement of Technology (KIAT) and Establishment of Infrastructure for Industrialization of Korean Useful Microbes (R0004073).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals


Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

13213_2018_1424_MOESM1_ESM.docx (20 kb)
Table S1 (DOCX 19 kb)
13213_2018_1424_MOESM2_ESM.docx (17 kb)
Table S2 (DOCX 17 kb)


  1. Adisakwattana S, Moonsan P, Yibchok-anun S (2008) Insulin-releasing properties of a series of cinnamic acid derivatives in vitro and in vivo. J Agric Food Chem 56:7838–7844. CrossRefPubMedGoogle Scholar
  2. Ashraf R, Vasiljevic T, Day SL, Smith SC, Donkor ON (2014) Lactic acid bacteria and probiotic organisms induce different cytokine profile and regulatory T cells mechanisms. J Funct Foods 6:395–409. CrossRefGoogle Scholar
  3. Bautista-Gallego J, Arroyo-López FN, Rantsiou K, Jiménez-Díaz R, Garrido-Fernández A, Cocolin L (2013) Screening of lactic acid bacteria isolated from fermented table olives with probiotic potential. Food Res Int 50:135–142. CrossRefGoogle Scholar
  4. Cao Z, Pan H, Tong H, Gu D, Li S et al (2016) In vitro evaluation of probiotic potential of Pediococcus pentosaceus L1 isolated from paocai—a Chinese fermented vegetable. Ann Microbiol 66:963–971. CrossRefGoogle Scholar
  5. Casarotti SN, Carneiro BM, Todorov SD, Nero LA, Rahal P et al (2017) In vitro assessment of safety and probiotic potential characteristics of Lactobacillus strains isolated from water buffalo mozzarella cheese. Ann Microbiol 67:289–301. CrossRefGoogle Scholar
  6. Couteau D, McCartney AL, Gibson GR, Williamson G, Faulds CB (2001) Isolation and characterization of human colonic bacteria able to hydrolyse chlorogenic acid. J Appl Microbiol 90:873–881. CrossRefPubMedGoogle Scholar
  7. Del Re B, Sgorbati B, Miglioli M, Palenzona D (2000) Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett Appl Microbiol 31:438–442. CrossRefPubMedGoogle Scholar
  8. Donaghy J, Kelly PF, McKay AM (1998) Detection of ferulic acid esterase production by Bacillus spp. and Lactobacilli. Appl Microbiol Biotechnol 50:257–260. CrossRefPubMedGoogle Scholar
  9. FAO/WHO (2001) Report on joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Accessed at 7 June 2015
  10. Greene JD, Klaenhammer TR (1994) Factors involved in adherence of lactobacilli to human Caco-2 cells. Appl Environ Microbiol 60:4487–4494PubMedPubMedCentralGoogle Scholar
  11. Guan L, Cho KH, Lee JH (2011) Analysis of the cultivable bacterial community in jeot-gal, a Korean salted and fermented seafood, and identification of its dominant bacteria. Food Microbiol 28:101–113. CrossRefPubMedGoogle Scholar
  12. Kim JH, Baik SH (2015) Preparation and characterization of fermented dandelion (Taraxacum officinale) beverage using Lactobacillus acidophilus F46 having cinnamoyl esterase activity. Food Sci Biotechnol 24:583–593. CrossRefGoogle Scholar
  13. Kim SJ, Ma SJ, Kim HL (2005) Probiotic properties of lactic acid bacteria and yeasts isolated from Korean traditional food, jeot-gal. Korean J Food Preserv 12:184–189Google Scholar
  14. Lai KK, Lorca GL, Gonzalez CF (2009) Biochemical properties of two cinnamoyl esterases purified from a Lactobacillus johnsonii strain isolated from stool samples of diabetes-resistant rats. Appl Environ Microbiol 75:5018–5024. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Maassen CB, van Holten-Neelen C, Balk F, den Bak-Glashouwer MJH, Leer RJ et al (2000) Strain-dependent induction of cytokine profiles in the gut by orally administered Lactobacillus strains. Vaccine 18:2613–2623. CrossRefPubMedGoogle Scholar
  16. Matsuzaki T, Yamazaki R, Hashimoto S, Yokokura T (1998) The effect of oral feeding of Lactobacillus casei strain Shirota on immunoglobulin E production in mice. J Dairy Sci 81:48–53. CrossRefPubMedGoogle Scholar
  17. Monteagudo-Mera A, Rodríguez-Aparicio L, Rua J, Matinez-Blanco H, Nacasa N (2012) In vitro evaluation of physiological probiotic properties of different lactic acid bacteria strains of dairy and human origin. J Funct Foods 4:531–541. CrossRefGoogle Scholar
  18. Olthof MR, Hollman PCH, Katan MB (2001) Chlorogenic acid and caffeic acid are absorbed in humans. J Nutr 131:66–71. CrossRefPubMedGoogle Scholar
  19. Palachum W, Chisti Y, Choorit W (2018) In-vitro assessment of probiotic potential of Lactobacillus plantarum WU-P19 isolated from a traditional fermented herb. Ann Microbiol 68:79–91. CrossRefGoogle Scholar
  20. Perdigon G, Galdeano CM, Valdez JC, Medici M (2002) Interaction of lactic acid bacteria with the gut immune system. Eur J Clin Nutr 56:S21. CrossRefPubMedGoogle Scholar
  21. Pochard P, Gosset P, Grangette C, Andre C, Tonnel AB (2002) Lactic acid bacteria inhibit Th2 cytokine production by mononuclear cells from allergic patients. J Allergy Clin Immunol 110:617–623. CrossRefPubMedGoogle Scholar
  22. Raimondi S, Anighoro A, Quartieri A, Amaretti A, Tomas-Barberan FA (2015) Role of bifidobacteria in the hydrolysis of chlorogenic acid. Microbiol Open 4:41–52. CrossRefGoogle Scholar
  23. Ramos CL, Thorsen L, Schwan RF, Jespersen L (2013) Strain-specific probiotics properties of Lactobacillus fermentum, Lactobacillus plantarum and Lactobacillus brevis isolates from Brazilian food products. Food Microbiol 36:22–29. CrossRefPubMedGoogle Scholar
  24. Rodes L, Khan A, Paul A, Coussa-Charley M, Marinescu D et al (2013) Effect of probiotics Lactobacillus and Bifidobacterium on gut-derived lipopolysaccharides and inflammatory cytokines: an in vitro study using a human colonic microbiota model. J Microbiol Biotechnol 23:518–526. CrossRefPubMedGoogle Scholar
  25. Roesch LF, Lorca GL, Casella G, Giongo A, Naranjo A et al (2009) Culture-independent identification of gut bacteria correlated with the onset of diabetes in a rat model. ISME J 5:536–548. CrossRefGoogle Scholar
  26. Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9:29–33. CrossRefGoogle Scholar
  27. Sakaguchi S (2004) Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22:531–562.
  28. Samot J, Lebreton J, Badet C (2011) Adherence capacities of oral lactobacilli for potential probiotic purposes. Anaerobe 17:69–72. CrossRefPubMedGoogle Scholar
  29. Schillinger U, Guigas C, Holzapfel WH (2005) In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. Int Dairy J 15:1289–1297. CrossRefGoogle Scholar
  30. Servin AL, Coconnier MH (2003) Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract Res Clin Gastroenterol 17:741–754. CrossRefPubMedGoogle Scholar
  31. Solieri L, Bianchi A, Mottolese G, Lemmetti F, Giudici P (2014) Tailoring the probiotic potential of non-starter Lactobacillus strains from ripened Parmigiano Reggiano cheese by in vitro screening and principal component analysis. Food Microbiol 38:240–249. CrossRefPubMedGoogle Scholar
  32. Tambekar DH, Bhutada SA (2010) Studies on antimicrobial activity and characteristics of bacteriocins produced by Lactobacillus strains isolated from milk of domestic animals. Int J Microbiol 8:1–6Google Scholar
  33. Tulumoglu S, Yuksekdag ZN, Beyatli Y, Simsek O, Cinar B et al (2013) Probiotic properties of lactobacilli species isolated from children’s feces. Anaerobe 24:36–42. CrossRefPubMedGoogle Scholar
  34. Wang CY, Lin PR, Ng CC, Shyu YT (2010) Probiotic properties of lactobacillus strains isolated from the feces of breast-fed infants and Taiwanese pickled cabbage. Anaerobe 16:578–585. CrossRefPubMedGoogle Scholar
  35. Wang J, Yang K, Liu M, Zhang J, Wei X et al (2018) Screening for potential probiotic from spontaneously fermented non-dairy foods based on in vitro probiotic and safety properties. Ann Microbiol 68:s13213-018-1386-3. CrossRefGoogle Scholar
  36. Wu C, He G, Zhang J (2014) Physiological and proteomic analysis of Lactobacillus casei in response to acid adaptation. J Ind Microbiol Biotechnol 41:1533–1540. CrossRefPubMedGoogle Scholar

Copyright information

© Università degli studi di Milano 2019

Authors and Affiliations

  1. 1.Department of Food Science and Human NutritionChonbuk National UniversityJeonjuRepublic of Korea
  2. 2.Rural Development AdministrationNational Institutes of Animal ScienceWanjuRepublic of Korea

Personalised recommendations