Log in

Safety evaluation and anti-inflammatory activity of Lactobacillus johnsonii IDCC 9203 isolated from feces of breast-fed infants

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

This study evaluated the safety of Lactobacillus johnsonii IDCC 9203 and investigated its anti-inflammatory activity in lipopolysaccharide (LPS)-induced RAW 264.7 macrophages. Genomic analysis revealed that this strain has no virulence and antibiotic resistance gene except tetW, which is a tetracycline resistance gene. Minimum inhibitory concentration data showed that the strain is resistant to tetracycline and aminoglycosides. Further analysis indicated that the transferability of the tetW gene is extremely low, and resistance to aminoglycosides is due to the intrinsic resistance of L. johnsonii IDCC 9203. Phenotypic safety assessment showed that the strain has neither β-hemolytic nor β-glucuronidase activity, and no biogenic amine production. When LPS-induced RAW 264.7 cells were treated with L. johnsonii IDCC 9203, the level of nitric oxide and expression of pro-inflammatory cytokines significantly decreased (p < 0.05). Therefore, L. johnsonii IDCC 9203 strain is considered as safe and beneficial probiotic for human consumption.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Data availability and materials

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abriouel H, Perez-Montoro B, Casado-Munoz MC, Knapp CW, Galvez A, Benomar N (2017) In silico genomic insights into aspects of food safety and defense mechanisms of a potentially probiotic Lactobacillus pentosus MP-10 isolated from brines of naturally fermented Alorena green table olives. PLoS ONE 12:e0176801

    Article  Google Scholar 

  • Allain T, Chaouch S, Thomas M, Vallée I, Buret AG, Langella P, Grellier P, Polack B, Bermúdez-Humarán LG, Florent I (2018) Bile-salt-hydrolases from the probiotic strain Lactobacillus johnsonii La1 mediate anti-giardial activity in vitro and in vivo. Front Microbiol 8:2707

    Article  Google Scholar 

  • Arndt D, Grant J, Marcu A, Sajed T, Pon A, Liang Y, Wishart DS (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44:16–21

    Article  Google Scholar 

  • Biagioli M, Laghi L, Carino A, Cipriani S, Distrutti E, Marchianò S, Parolin C, Scarpelli P, Vitali B, Fiorucci S (2017) Metabolic variability of a multispecies probiotic preparation impacts on the anti-inflammatory activity. Front Pharmacol 8:505

    Article  Google Scholar 

  • Byakika S, Mukisa IM, Byaruhanga YB, Muyanja C (2019) A review of criteria and methods for evaluating the probiotic potential of microorganisms. Food Rev Int 35:427–466

    Article  CAS  Google Scholar 

  • Castro-Lopez C, García HS, Martínez-Avila GCG, Gonzalez-Cordova AF, Vallejo-Cordoba B, Hernandez-Mendoza A (2021) Genomics-based approaches to identify and predict the health-promoting and safety activities of promising probiotic strains – A probiogenomics review. Trends Food Sci Technol 108:148–163. https://doi.org/10.1016/j.tifs.2020.12.017

    Article  CAS  Google Scholar 

  • Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, ** Q (2005) VFDB: a reference database for bacterial virulence factors. Nucl Acids Res 33:325–328

    Article  Google Scholar 

  • Davoren MJ, Liu J, Castellanos J, Rodríguez-Malavé NI, Schiestl RH (2019) A novel probiotic, Lactobacillus johnsonii 456, resists acid and can persist in the human gut beyond the initial ingestion period. Gut Microbes 10:458–480

    Article  CAS  Google Scholar 

  • Devi SM, Kurrey NK, Halami PM (2018) In vitro anti-inflammatory activity among probiotic Lactobacillus species isolated from fermented foods. J Funct Foods 47:19–27

    Article  CAS  Google Scholar 

  • DiMarzio M, Rusconi B, Yennawar NH, Ep**er M, Patterson AD, Dudley EG (2017) Identification of a mouse Lactobacillus johnsonii strain with deconjugase activity against the FXR antagonist T-β-MCA. PLoS ONE 12(9):e0183564

    Article  Google Scholar 

  • EFSA (2018) Guidance on the characterization of microorganisms used as feed additives or as production organisms. EFSA J 16(3):5206

    Google Scholar 

  • FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food. London Ontario, Canada. https://www.mhlw.go.jp/file/05-Shingikai-11121000-Iyakushokuhinkyoku-Soumuka/0000197343.pdf. Accessed 10 July 2022

  • Hu SS, Bradsh aw HB, Ch en JS, Tan B, Walker JM, (2008) Prostaglandin E 2 glycerol ester, an endogenous COX-2 metabolite of 2-arachidonoylglycerol, induces hyperalgesia and modulates NFκB activity. Br J Pharmacol 153:1538–1549

    Article  CAS  Google Scholar 

  • Jahan M, Zhanel GG, Sparling R, Holley RA (2015) Horizontal transfer of antibiotic resistance from Enterococcus faecium of fermented meat origin to clinical isolates of E. faecium and Enterococcus faecalis. Int J Food Microbiol 199:78–85

  • Je IG, Lee DG, Jeong DG, Hong D, Yoon JM, Moon JS, Park S (2018) The probiotic, ID-JPL934, attenuates dextransulfate sodium-induced colitis in mice through inhibition of proinflammatory cytokines expression. J Med Food 21:858–865

    Article  CAS  Google Scholar 

  • Kim SB, Kang BH, Kwon HS, Kang JH (2011) Antiinflammatory and antiallergic activity of fermented turmeric by Lactobacillus johnsonii IDCC 9203. Korean J Microbiol Biotechnol 39:266–273

    CAS  Google Scholar 

  • Kim T, Lee B, Kwon H, Moon JS, Choi SK (2019) Complete genome sequence of probiotic Lactobacillus johnsonii IDCC9203 isolated from infant feces. Korean J Microbiol 55:432–435

    Google Scholar 

  • Lee SH, Yang EH, Kwon HS, Kang JH, Kang BH (2008) Potential Probiotic Properties of Lactobacillus johnsonii IDCC 9203 Isolated from Infant Feces. Korean J Microbiol Biotechnol 36:121–127

    CAS  Google Scholar 

  • Li T, Teng D, Mao R, Hao Y, Wang X, Wang J (2020) A critical review of antibiotic resistance in probiotic bacteria. Food Res Int 136:109571

    Article  CAS  Google Scholar 

  • Liu B, Pop M (2009) ARDB-antibiotic resistance genes database. Nucleic Acids Res 37:443–447

    Article  Google Scholar 

  • Maresca D, Zotta T, Mauriello G (2018) Adaptation to aerobic environment of Lactobacillus johnsonii/gasseri strains. Front Microbiol 9:157

    Article  Google Scholar 

  • McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, Kalan L (2013) The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57:3348–3357

    Article  CAS  Google Scholar 

  • OECD (2008) Test No. 425: acute oral toxicity: up-and-down procedure. OECD Guidelines for the Testing of Chemicals, Section 4, Part 425. OECD Publishing, Paris

  • Polit A, Yang HY, Amund D (2018) Investigating the transmissibility of tet(W) in bifidobacteria exposed to acid and bile stress. Biosci Microbiota Food Health 37:39–43

    Article  CAS  Google Scholar 

  • Qureshi N, Gu Q, Li P (2020) Whole genome sequence analysis and in vitro probiotic characteristics of a Lactobacillus strain Lactobacillus paracasei ZFM54. J Appl Microbiol 129:422–433

    Article  CAS  Google Scholar 

  • Rozman V, Lorbeg PM, Accetto T, Matijasic BB (2020) Characterization of antimicrobial resistance in lactobacilli and bifidobacteria used as probiotics or starter cultures based on integration of phenotypic and in silico data. Int J Food Microbiol 314:108388

    Article  CAS  Google Scholar 

  • Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H (2010) Biogenic amines in fermented foods. Eur J Clin Nutr 64:95–100

    Article  Google Scholar 

  • Suzzi G, Torriani S (2015) Editorial: Biogenic amines in foods. Front Microbiol 6:472

    Article  Google Scholar 

  • Tarrah A, Pakroo S, Corich V, Giacomini A (2020) Whole-genome sequence and comparative genome analysis of Lactobacillus paracasei DTA93, a promising probiotic lactic acid bacterium. Arch Microbiol 202:1997–2003

    Article  CAS  Google Scholar 

  • Wu X, Zhao C, Guo Z, Hao Y, Li J, Shi H, Sun Y (2016) Genome sequence of Lactobacillus johnsonii strain W1, isolated from mice. Genome Announc 4:e00561-e616

    PubMed  PubMed Central  Google Scholar 

  • Yan F, Polk DB (2020) Probiotics and probiotic-derived functional factors—mechanistic insights into applications for intestinal homeostasis. Front Immunol 11:1428. https://doi.org/10.3389/fimmu.2020.01428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu H, Lee N, Choi A, Choe J, Bae CH, Paik H (2019) Anti-inflammatory potential of probiotic strain Weissella cibaria JW15 isolated from kimchi through regulation of NF-κB and MAPKs pathways in LPS-induced RAW 264 7 cells. J Microbiol Biotechnol 29(7):1022–1032

    Article  CAS  Google Scholar 

  • Zhang W, Wang J, Zhang D, Liu H, Wang S, Wang Y, Ji H (2019) Complete genome sequencing and comparative genome characterization of Lactobacillus johnsonii ZLJ010, a potential probiotic with health-promoting properties. Front Genet 10:812

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Research Foundation of Korea grant funded by the Korean government (Ministry of Science and ICT, MSIT; grant no. 2020R1C1C1005251), and Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry (IPET) through High Value-added Food Technology Development Program, funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA) (321033–3).

Author information

Authors and Affiliations

Authors

Contributions

OEA conducted statistical analysis, interpreted the data, and wrote the draft manuscript. SAC performed experiment, conducted statistical analysis, and interpreted the data. OB, WYB, HK, and HJJ performed part of the experiment. CEC reviewed and revised the draft manuscript. JY and YHJ conceived the idea, acquired fund, supervised the project, reviewed, and revised the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jungwoo Yang or Young Hoon Jung.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Ethical approval

Animal studies were conducted at the Korea Testing and Research Institute (KTRI; Hwasun-gun, Jeollanam-do, Korea) under the Animal Protection Act (no. 14651) and Laboratory Animal Act (no. 15278) of the Korean government.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 920 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Adedeji, O.E., Chae, S.A., Ban, OH. et al. Safety evaluation and anti-inflammatory activity of Lactobacillus johnsonii IDCC 9203 isolated from feces of breast-fed infants. Arch Microbiol 204, 470 (2022). https://doi.org/10.1007/s00203-022-03097-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-022-03097-0

Keywords

Navigation