Advertisement

Adhesion-Related Immunomodulatory Activity of the Screened Lactobacillus plantarum from Sichuan Pickle

  • Shanshan Chen
  • Pei Cao
  • Fengxuan Lang
  • Zhen Wu
  • Daodong Pan
  • Xiaoqun Zeng
  • Liwei Lian
Article
  • 11 Downloads

Abstract

Lactic acid bacteria are the majority fermentation starter in the traditional fermented foods. In this research, a promising Lactobacillus plantarum was isolated from Sichuan pickle and its adhesion properties were analyzed in simulated gastrointestinal fluid with different methods. Meanwhile, the immunomodulatory effect of this strain was also evaluated in the Caco-2 cells. Results found that adhesion-related mub genes and other genes like lsp and tuf were upregulated in different culture times. Furthermore, L. plantarum cultured at alkaline environment revealed some anti-inflammation activity through inhibited expression of cytokine IL-8 and increased expression of anti-inflammatory cytokine IL-10 in Caco-2 cells. The texture of yogurt after fermented by this kind of isolated strain was also investigated, which provides the foundation for the further development and application of this kind of strain in food production. More investigations need to be carried out to determine whether this probiotic contributes to regulation of intestinal flora and prevention of gut inflammation.

Notes

Acknowledgements

This work was supported by the Natural Science Funding of China (31671869, 31601487, 31471598), the Natural Science Funding of Zhejiang (LY19C200005), the Science and Technology Bureau of Ningbo (2016C10022), Open Funding of the Key Laboratory of Animal Protein Deep Processing Technology of Zhejiang (ZX2015000928), and the K. C. Wong Magna Fund in Ningbo University.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interests.

Supplementary material

284_2018_1580_MOESM1_ESM.docx (14 kb)
Supplementary material 1 (DOCX 13 KB)

References

  1. 1.
    Abushelaibi A, Al-Mahadin S, El-Tarabily K, Shah NP, Ayyash M (2017) Characterization of potential probiotic lactic acid bacteria isolated from camel milk. LWT-Food Sci Technol 79:316–325.  https://doi.org/10.1016/j.lwt.2017.01.041 CrossRefGoogle Scholar
  2. 2.
    Ali NM, Yeap SK, Yusof HM, Beh BK, Ho WY, Koh SP et al (2016) Comparison of free amino acids, antioxidants, soluble phenolic acids, cytotoxicity and immunomodulation of fermented mung bean and soybean. J Sci Food Agric 96:1648–1658.  https://doi.org/10.1002/jsfa.7267 CrossRefPubMedGoogle Scholar
  3. 3.
    Altamimi M, Abdelhay O, Rastall RA (2016) Effect of oligosaccharides on the adhesion of gut bacteria to human HT-29 cells. Anaerobe 39:136–142.  https://doi.org/10.1016/j.anaerobe.2016.03.010 CrossRefPubMedGoogle Scholar
  4. 4.
    Champagne CP, Raymond Y, Guertin N, Martoni CJ, Jones ML, Mainville I et al (2015) Impact of a yogurt matrix and cell microencapsulation on the survival of Lactobacillus reuteri in three in vitro gastric digestion procedures. Benef Microbes 6:753–763.  https://doi.org/10.3920/BM2014.0162 CrossRefPubMedGoogle Scholar
  5. 5.
    Chen L, Zhang QH, Ji Z, Shu GW, Chen H (2018) Production and fermentation characteristics of Angiotensin-I-converting enzyme inhibitory peptides of goat milk fermented by a novel wild Lactobacillus plantarum 69. LWT-Food Sci Technol 91:532–540.  https://doi.org/10.1016/j.lwt.2018.02.002 CrossRefGoogle Scholar
  6. 6.
    Deepika G, Karunakaran E, Hurley CR, Biggs CA, Charalampopoulos D (2012) Influence of fermentation conditions on the surface properties and adhesion of Lactobacillus rhamnosus GG. Microb Cell Fact 11:116.  https://doi.org/10.1186/1475-2859-11-116 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Ejtahed HS, Soroush AR, Angoorani P, Larijani B, Hasani-Ranjbar S (2016) Gut microbiota as a target in the pathogenesis of metabolic disorders: a new approach to novel therapeutic agents. Horm Metab Res 48:349–358.  https://doi.org/10.1055/s-0042-107792 CrossRefPubMedGoogle Scholar
  8. 8.
    Greene JD, Klaenhammer TR (1994) Factors involved in adherence of lactobacilli to human Caco-2 cells. Appl Environ Microb 60:4487Google Scholar
  9. 9.
    Ilha EC, da Silva T, Lorenz JG, Rocha GD, Sant’Anna ES (2015) Lactobacillus paracasei isolated from grape sourdough: acid, bile, salt, and heat tolerance after spray drying with skim milk and cheese whey. Eur Food Res Technol 240:977–984.  https://doi.org/10.1007/s00217-014-2402-x CrossRefGoogle Scholar
  10. 10.
    Jia FF, Zhang LJ, Pang XH, Gu XX, Abdelazez A, Liang Y et al (2017) Complete genome sequence of bacteriocin-producing Lactobacillus plantarum KLDS1.0391, a probiotic strain with gastrointestinal tract resistance and adhesion to the intestinal epithelial cells. Genomics 109:432–437.  https://doi.org/10.1016/j.ygeno.2017.06.008 CrossRefPubMedGoogle Scholar
  11. 11.
    Johnson-Henry KC, Hagen KE, Gordonpour M, Tompkins TA, Sherman PM (2007) Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cell Microbiol 9:356–367.  https://doi.org/10.1111/j.1462-5822.2006.00791.x CrossRefPubMedGoogle Scholar
  12. 12.
    Jose NM, Bunt CR, McDowell A, Chiu JZS, Hussain MA (2017) Short communication: a study of Lactobacillus isolates’ adherence to and influence on membrane integrity of human Caco-2 cells. J Dairy Sci 100:7891–7896.  https://doi.org/10.3168/jds.2017-12912 CrossRefPubMedGoogle Scholar
  13. 13.
    Koskenniemi K, Laakso K, Koponen J, Kankainen M, Greco D, Auvinen P et al (2011) Proteomics and transcriptomics characterization of bile stress response in probiotic Lactobacillus rhamnosus GG. Mol Cell Proteom 10:M110.002741.  https://doi.org/10.1074/mcp.M110.002741 CrossRefGoogle Scholar
  14. 14.
    Lievin-Le Moal V, Servin AL (2014) Anti-infective activities of Lactobacillus strains in the human intestinal microbiota: from probiotics to gastrointestinal anti-infectious biotherapeutic agents. Clin Microbiol Rev 27:167–199.  https://doi.org/10.1128/CMR.00080-13 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Liong MT, Shah NP (2005) Acid and bile tolerance and cholesterol removal ability of lactobacilli strains. J Dairy Sci 88:55–66.  https://doi.org/10.3168/jds.S0022-0302(05)72662-X CrossRefPubMedGoogle Scholar
  16. 16.
    Połka J, Rebecchi A, Pisacane V, Morelli L, Puglisi E (2015) Bacterial diversity in typical italian salami at different ripening stages as revealed by high-throughput sequencing of 16 s rRNA amplicons. Food Microbiol 46:342–356.  https://doi.org/10.1016/j.fm.2014.08.023 CrossRefPubMedGoogle Scholar
  17. 17.
    Ramiah K, Reenen CAV, Dicks LMT (2007) Expression of the mucus adhesion genes Mub and MapA, adhesion-like factor EF-Tu and bacteriocin gene plaA of Lactobacillus plantarum 423, monitored with real-time PCR. Int J Food Microbiol 116:405–409.  https://doi.org/10.1016/j.ijfoodmicro.2007.02.011 CrossRefPubMedGoogle Scholar
  18. 18.
    Ranadheera CS, Evans CA, Adams MC, Baines SK (2014) Effect of dairy probiotic combinations on in vitro gastrointestinal tolerance, intestinal epithelial cell adhesion and cytokine secretion. J Funct Foods 8:18–25.  https://doi.org/10.1016/j.jff.2014.02.022 CrossRefGoogle Scholar
  19. 19.
    Roos S, Jonsson H (2002) A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 148:433–442.  https://doi.org/10.1099/00221287-148-2-433 CrossRefPubMedGoogle Scholar
  20. 20.
    Succi M, Pannella G, Tremonte P, Tipaldi L, Coppola R, Iorizzo M et al (2017) Sub-optimal pH preadaptation improves the survival of Lactobacillus plantarum strains and the malic acid consumption in wine-like medium. Front Microbiol 8:470.  https://doi.org/10.3389/fmicb.2017.00470 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Todorov SD, Dicks LMT (2008) Evaluation of lactic acid bacteria from kefir, molasses and olive brine as possible probiotics based on physiological properties. Ann Microbiol 58:661–670.  https://doi.org/10.1007/BF03175572 CrossRefGoogle Scholar
  22. 22.
    Tuomola EM, Ouwehand AC, Salminen SJ (2000) Chemical, physical and enzymatic pre-treatments of probiotic lactobacilli alter their adhesions to human intestinal mucus glycoproteins. Int J Food Microbiol 60:75–81.  https://doi.org/10.1016/S0168-1605(00)00319-6 CrossRefPubMedGoogle Scholar
  23. 23.
    Wang R, Jiang L, Zhang M, Zhao L, Hao YL, Guo HY et al (2017) The adhesion of Lactobacillus salivarius REN to a human intestinal epithelial cell line requires S-layer proteins. Sci Rep 7:44029.  https://doi.org/10.1038/srep44029 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Wang WW, He JY, Pan DD, Wu Z, Guo YX, Zeng XQ et al (2018) Metabolomics analysis of Lactobacillus plantarum ATCC 14917 adhesion activity under initial acid and alkali stress. PLoS ONE 13(5):e0196231.  https://doi.org/10.1371/journal.pone.0196231 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Yu J, Gao W, Qing MJ, Sun ZH, Wang WH, Liu WJ et al (2012) Identification and characterization of lactic acid bacteria isolated from traditional pickles in Sichuan. China J Gen Appl Microbiol 58:163–172.  https://doi.org/10.2323/jgam.58.163 CrossRefPubMedGoogle Scholar
  26. 26.
    Zivkovic M, Miljkovic MS, Ruas-Madiedo P, Markelic MB, Veljovic K, Tolinacki M et al (2016) EPS-SJ exopolisaccharide produced by the strain Lactobacillus paracasei subsp paracasei BGSJ2-8 is involved in adhesion to epithelial intestinal cells and decrease on E-coil association to Caco-2 cells. Front Microbiol 7:00286.  https://doi.org/10.3389/fmicb.2016.00286 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Animal Protein Deep Processing Technology of Zhejiang, School of Food and Pharmaceutical ScienceNingbo UniversityNingboPeople’s Republic of China
  2. 2.Department of Food Science & NutritionGinling College, Nanjing Normal UniversityNanjingPeople’s Republic of China
  3. 3.Ningbo Dairy GroupNingboPeople’s Republic of China

Personalised recommendations