Skip to main content

Advertisement

SpringerLink
Log in

Probiotic Pediococcus acidilactici strain from tomato pickle displays anti-cancer activity and alleviates gut inflammation in-vitro

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

The present study characterized the potential probiotic properties of Pediococcus acidilactici TMAB26 strain isolated from traditional Indian tomato pickle, and evaluated its possible therapeutic applications as an anti-cancer and anti-inflammatory agent in vitro. The 16S rRNA sequencing and primary screening demarcated TMAB26 strain as an ideal probiotic candidate, with distinctive properties of acid tolerance (58.02% at pH 2.5), bile tolerance (55.53% at 0.5%), and efficient adherence to the mucosal surface of the human intestinal cells in vitro, along with antagonistic, anti-inflammatory, and anti-cancer properties. The strain exhibited antagonism against standard intestinal pathogenic strains Staphylococcus aureus, Pseudomonas aeruginosa, Bacillus subtilis, E. coli, Klebsiella pneumonia, and Salmonella typhi with zones of inhibition in the range of 6–18 mm. The cytotoxicity evaluation of the probiotic isolate TMAB26 culture supernatant (1:1 dilution) showed significant cytotoxicity on HT-29 (94.91% ± 1.27) and Caco-2 (92.63% ± 0.63) cancer cells when compared to that of the peripheral blood mononuclear cells (PBMCs) alone. Furthermore, the strain culture supernatant reduced the mRNA levels of the proinflammatory cytokine tumor necrosis factor-alpha (TNF-α) by threefold, Interleukin-6 (IL-6) by eightfold and increased the mRNA levels of the anti-inflammatory cytokine Interleukin-10 (IL-10) in lipopolysaccharide (LPS) pretreated HT-29 and peripheral blood mononuclear cells (PBMCs), suggesting the potential role of TMAB26 isolate, i.e., Pediococcus acidilactici MTCC 13014 in alleviating gut inflammation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Al Obeed OA, Alkhayal KA, Al Sheikh A, Zubaidi AM, Vaali-Mohammed M-A, Boushey R, Mckerrow JH, Abdulla M-H (2014) Increased expression of tumor necrosis factor-α is associated with advanced colorectal cancer stages. World J Gastroenterol WJG 20:18390

    Article  CAS  Google Scholar 

  • Attri P, Jodha D, Gandhi D, Chanalia P, Dhanda S (2015) In vitro evaluation of Pediococcus acidilactici NCDC 252 for its probiotic attributes. Int J dairy Technol 68:533–542

    Article  CAS  Google Scholar 

  • Borges S, Barbosa J, Silva J, Teixeira P (2013) Evaluation of characteristics of Pediococcus spp. to be used as a vaginal probiotic. J Appl Microbiol 115:527–538

    Article  CAS  Google Scholar 

  • Carol M, Borruel N, Antolin M, Llopis M, Casellas F, Guarner F, Malagelada JR (2006) Modulation of apoptosis in intestinal lymphocytes by a probiotic bacteria in Crohn’s disease. J Leukoc Biol 79:917–922

    Article  CAS  Google Scholar 

  • Chau I, Cunningham D (2006) Adjuvant therapy in colon cancer—what, when and how? Ann Oncol 17:1347–1359

    Article  CAS  Google Scholar 

  • Choi A-R, Patra JK, Kim WJ, Kang S-S (2018) Antagonistic activities and probiotic potential of lactic acid bacteria derived from a plant-based fermented food. Front Microbiol 9:1963

    Article  Google Scholar 

  • Chon H, Choi B, Lee E, Lee S, Jeong G (2009) Immunomodulatory effects of specific bacterial components of Lactobacillus plantarum KFCC11389P on the murine macrophage cell line RAW 264· 7. J Appl Microbiol 107:1588–1597

    Article  CAS  Google Scholar 

  • Collins MD, Gibson GR (1999) Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. Am J Clin Nutr 69:1052s–1057s

    Article  CAS  Google Scholar 

  • Cui W, Taub DD, Gardner K (2007) qPrimerDepot: a primer database for quantitative real time PCR. Nucleic Acids Res 35:D805–D809

    Article  CAS  Google Scholar 

  • Dallal MMS, Mojarrad M, Baghbani F, Raoofian R, Mardaneh J, Salehipour Z (2015) Effects of probiotic Lactobacillus acidophilus and Lactobacillus casei on colorectal tumor cells activity (CaCo-2). Arch Iran Med 18:167–172

  • de Ribeiro MC, O, Vandenberghe LP de S, Spier MR, Paludo KS, Soccol CR, Soccol VT, (2014) Evaluation of probiotic properties of Pediococcus acidilactici B14 in association with Lactobacillus acidophilus ATCC 4356 for application in a soy based aerated symbiotic dessert. Brazil Arch Biol Technol 57:755–765

    Article  Google Scholar 

  • Delgado S, O’sullivanFitzgeraldMayo EGB (2007) Subtractive screening for probiotic properties of Lactobacillus species from the human gastrointestinal tract in the search for new probiotics. J Food Sci 72:M310–M315

    Article  CAS  Google Scholar 

  • Dowarah R, Verma AK, Agarwal N, Singh P, Singh BR (2018) Selection and characterization of probiotic lactic acid bacteria and its impact on growth, nutrient digestibility, health and antioxidant status in weaned piglets. PLoS ONE 13(3):e0192978

    Article  Google Scholar 

  • Duary RK, Rajput YS, Batish VK, Grover S (2011) Assessing the adhesion of putative indigenous probiotic lactobacilli to human colonic epithelial cells. Indian J Med Res 134:664

    Article  CAS  Google Scholar 

  • Duary RK, Batish VK, Grover S (2014) Immunomodulatory activity of two potential probiotic strains in LPS-stimulated HT-29 cells. Genes Nutr 9:398

    Article  Google Scholar 

  • Gómez NC, Ramiro JMP, Quecan BXV, de Melo Franco BDG (2016) Use of potential probiotic lactic acid bacteria (LB) biofilms for the control of Listeria monocytogenes, Salmonella typhimurium, and Escherichia coli O157: H7 biofilms formation. Front Microbiol 7:863

    Article  Google Scholar 

  • Kim SH, Kim WJ, Kang SS (2019) Inhibitory effect of bacteriocin-producing Lactobacillus brevis DF01 and Pediococcus acidilactici K10 isolated from kimchi on enteropathogenic bacterial adhesion. Food Bioscience 30:100425

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  Google Scholar 

  • Ladha G, Jeevaratnam K (2020) Characterization of purified antimicrobial peptide produced by Pediococcus pentosaceus LJR1, and its application in preservation of white leg shrimp. World J Microbiol Biotechnol 36:1–12

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Menard S, Candalh C, Bambou JC, Terpend K, Cerf-Bensussan N, Heyman M (2004) Lactic acid bacteria secrete metabolites retaining anti-inflammatory properties after intestinal transport. Gut 53:821–828

    Article  CAS  Google Scholar 

  • Mendes MCS, Paulino DSM, Brambilla SR, Camargo JA, Persinoti GF, Carvalheira JBC (2018) Microbiota modification by probiotic supplementation reduces colitis associated colon cancer in mice. World J Gastroenterol 24:1995

    Article  CAS  Google Scholar 

  • Mousavi ZE, Mousavi SM, Razavi SH, Emam-Djomeh Z, Kiani H (2011) Fermentation of pomegranate juice by probiotic lactic acid bacteria. World J Microbiol Biotechnol 27:123–128

    Article  CAS  Google Scholar 

  • Nagpal R, Kumar A, Kumar M, Behare PV, Jain S, Yadav H (2012) Probiotics, their health benefits and applications for developing healthier foods: a review. FEMS Microbiol Lett 334:1–15

    Article  CAS  Google Scholar 

  • Nouri Z, Karami F, Neyazi N, Modarressi MH, Karimi R, Khorramizadeh MR, Taheri B, Motevaseli E (2016) Dual anti-metastatic and anti-proliferative activity assessment of two probiotics on HeLa and HT-29 cell lines. Cell J 18:127

    PubMed  PubMed Central  Google Scholar 

  • Pino A, De Angelis M, Chieppa M, Caggia C, Randazzo CL (2020) Gut microbiota, probiotics and colorectal cancer: a tight relation. WCRJ 7:1456

    Google Scholar 

  • Plaza-Díaz J, Ruiz-Ojeda FJ, Vilchez-Padial LM, Gil A (2017) Evidence of the anti-inflammatory effects of probiotics and synbiotics in intestinal chronic diseases. Nutrients 9:555

    Article  Google Scholar 

  • Plaza-Diaz J, Ruiz-Ojeda FJ, Gil-Campos M, Gil A (2019) Mechanisms of action of probiotics. Adv Nutr 10:S49–S66

    Article  Google Scholar 

  • Prakash J (2016) Probiotic effect on gastrointestinal flora. In: Prakash V, Martín-Belloso O, Keener L, Astley S, Braun S, Mcmahon H, Lelieveld H (eds) Regulating safety of traditional and ethnic foods. Academic Press, Elsevier Inc., p 536

  • Pringsulaka O, Rueangyotchanthana K, Suwannasai N, Watanapokasin R, Amnueysit P, Sunthornthummas S, Sukkhum S, Sarawaneeyaruk S, Rangsiruji A (2015) In vitro screening of lactic acid bacteria for multi-strain probiotics. Livest Sci 174:66–73

    Article  Google Scholar 

  • Rivera-Espinoza Y, Gallardo-Navarro Y (2010) Non-dairy probiotic products. Food Microbiol 27:1–11

    Article  Google Scholar 

  • Srisesharam S, Park HS, Soundharrajan I, Kuppusamy P, Kim DH, Jayraaj IA, Choi KC (2018) Evaluation of probiotic Lactobacillus plantarum against foodborne pathogens and its fermentation potential in improving Lolium multiflorum silage quality. 3 Biotech 10:8–443

    Google Scholar 

  • Tanaka T, Narazaki M (2014) Kishimoto T (2014) IL-6 in inflammation, immunity, and disease. Cold Spring Harb Perspect Biol 6:a016295

    Article  Google Scholar 

  • Vasiee A, Falah F, Behbahani BA, Tabatabaee-Yazdi F (2020) Probiotic characterization of Pediococcus strains isolated from Iranian cereal-dairy fermented product: interaction with pathogenic bacteria and the enteric cell line Caco-2. J Biosci Bioeng 130:471–479

  • Verna EC, Lucak S (2010) Use of probiotics in gastrointestinal disorders: what to recommend? Therap Adv Gastroenterol 3:307–319

    Article  Google Scholar 

  • Wang S, Yao B, Gao H, Zang J, Tao S, Zhang S, Huang S, He B, Wang J (2019) Combined supplementation of Lactobacillus fermentum and Pediococcus acidilactici promoted growth performance, alleviated inflammation, and modulated intestinal microbiota in weaned pigs. BMC Vet Res 15:239

    Article  Google Scholar 

  • Wang Y, Xie Q, Zhang Y, Ma W, Ning K, Xiang J-Y, Cui J, Xiang H (2020) Combination of probiotics with different functions alleviate DSS-induced colitis by regulating intestinal microbiota, IL-10, and barrier function. Appl Microbiol Biotechnol 104:335–349

    Article  CAS  Google Scholar 

  • Yadav M, Shukla P (2019) Recent systems biology approaches for probiotics use in health aspects: a review. 3 Biotech 12:9–448

    Google Scholar 

  • Yadav M, Shukla P (2020) Efficient engineered probiotics using synthetic biology approaches: a review. Biotechnol Appl Biochem 67:22–29

    Article  CAS  Google Scholar 

  • Yadav R, Puniya AK, Shukla P (2016) Probiotic properties of Lactobacillus plantarum RYPR1 from an indigenous fermented beverage Raabadi. Front Microbiol 7:1683

    PubMed  PubMed Central  Google Scholar 

  • Yadav R, Kumar V, Baweja M, Shukla P (2018) Gene editing and genetic engineering approaches for advanced probiotics: a review. Crit Rev Food Sci Nutr 58:1735–1746

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Authors are grateful to RUSA 2.0, MHRD, Govt. of India; Science and Engineering Research Board (SERB), Ministry of Science and Technology, Govt. of India (YSS/2015/000173, SB/EMEQ-258/2013) for their financial support and University Grants Commission (UGC), Govt. of India for providing fellowship to carry out this research work.

Funding

This study was funded by RUSA 2.0, MHRD, Govt. of India; Science and Engineering Research Board (SERB), Ministry of Science and Technology, Govt. of India (YSS/2015/000173, SB/EMEQ-258/2013).

Author information

Authors and Affiliations

  1. Centre for Microbial and Fermentation Technology, Department of Microbiology, University College of Science, Osmania University, Hyderabad, India

    Anuradha Barigela & Bhima Bhukya

Authors
  1. Anuradha Barigela
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bhima Bhukya
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AB designed all the experiments and carried out. BB designed the concept, monitored the experiments, and edited the manuscript prepared by AB. Both the authors read and approved the final manuscript.

Corresponding author

Correspondence to Bhima Bhukya.

Ethics declarations

Conflict of interest

Anuradha Barigela declares that she has no conflict of interest. Bhima Bhukya declares that he has no conflict of interest.

Human and animal rights

This article does not contain any studies with animals performed by any of the authors.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 16 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barigela, A., Bhukya, B. Probiotic Pediococcus acidilactici strain from tomato pickle displays anti-cancer activity and alleviates gut inflammation in-vitro. 3 Biotech 11, 23 (2021). https://doi.org/10.1007/s13205-020-02570-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-020-02570-1

Keywords

Search

Navigation