Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Anti-Tuberculosis Activity of Pediococcus acidilactici Isolated from Young Radish Kimchi against Mycobacterium tuberculosis

  • Yoon, Youjin (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University) ;
  • Seo, Hoonhee (Probiotics Microbiome Convergence Center, Soonchunhyang University) ;
  • Kim, Sukyung (Probiotics Microbiome Convergence Center, Soonchunhyang University) ;
  • Lee, Youngkyoung (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University) ;
  • Rahim, MD Abdur (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University) ;
  • Lee, Saebim (Probiotics Microbiome Convergence Center, Soonchunhyang University) ;
  • Song, Ho-Yeon (Department of Microbiology and Immunology, School of Medicine, Soonchunhyang University)
  • Received : 2021.07.27
  • Accepted : 2021.09.26
  • Published : 2021.12.28
Download PDF
⟨ Previous Next ⟩

Abstract

Tuberculosis is a highly contagious disease caused by Mycobacterium tuberculosis. It affects about 10 million people each year and is still one of the leading causes of death worldwide. About 2 to 3 billion people (equivalent to 1 in 3 people in the world) are infected with latent tuberculosis. Moreover, as the number of multidrug-resistant, extensively drug-resistant, and totally drug-resistant strains of M. tuberculosis continues to increase, there is an urgent need to develop new anti-tuberculosis drugs that are different from existing drugs to combat antibiotic-resistant M. tuberculosis. Against this background, we aimed to develop new anti-tuberculosis drugs using probiotics. Here, we report the anti-tuberculosis effect of Pediococcus acidilactici PMC202 isolated from young radish kimchi, a traditional Korean fermented food. Under coculture conditions, PMC202 inhibited the growth of M. tuberculosis. In addition, PMC202 inhibited the growth of drug-sensitive and -resistant M. tuberculosis- infected macrophages at a concentration that did not show cytotoxicity and showed a synergistic effect with isoniazid. In a 2-week, repeated oral administration toxicity study using mice, PMC202 did not cause weight change or specific clinical symptoms. Furthermore, the results of 16S rRNA-based metagenomics analysis confirmed that dysbiosis was not induced in bronchoalveolar lavage fluid after oral administration of PMC202. The anti-tuberculosis effect of PMC202 was found to be related to the reduction of nitric oxide. Our findings indicate that PMC202 could be used as an anti-tuberculosis drug candidate with the potential to replace current chemical-based drugs. However, more extensive toxicity, mechanism of action, and animal efficacy studies with clinical trials are needed.

Keywords

Acknowledgement

This study was funded by the Ministry of Trade, Industry and Energy (MOTIE), Korea, under the 'Regional Industry-Based Organization Support Program' (reference number P0001942) supervised by the Korea Institute for Advancement of Technology (KIAT). This research was also supported by Soonchunhyang University Research Fund.

References

  1. Orgeur M, Brosch R. 2018. Evolution of virulence in the Mycobacterium tuberculosis complex. Curr. Opin. Microbiol. 41: 68-75. https://doi.org/10.1016/j.mib.2017.11.021
  2. Koch A, Mizrahi V. 2018. Mycobacterium tuberculosis. Trends Microbiol. 26: 555-556. https://doi.org/10.1016/j.tim.2018.02.012
  3. Tarasuntisuk S, Palaga T, Kageyama H, Waditee-Sirisattha R. 2019. Mycosporine-2-glycine exerts anti-inflammatory and antioxidant effects in lipopolysaccharide (LPS)-stimulated RAW 264.7 macrophages. Arch. Biochem. Biophys. 662: 33-39. https://doi.org/10.1016/j.abb.2018.11.026
  4. Khawbung JL, Nath D, Chakraborty S. 2021. Drug resistant Tuberculosis: a review. Comp. Immunol. Microbiol. Infect. Dis. 74: 101574. https://doi.org/10.1016/j.cimid.2020.101574
  5. Chiang CY, Van Weezenbeek C, Mori T, Enarson DA. 2013. Challenges to the global control of tuberculosis. Respirology 18: 596-604. https://doi.org/10.1111/resp.12067
  6. Brust JCM, Shah NS, Mlisana K, Moodley P, Allana S, Campbell A, et al. 2018. Improved survival and cure rates with concurrent treatment for multidrug-resistant tuberculosis-human immunodeficiency virus coinfection in South Africa. Clin. Infect. Dis. 66: 1246-1253. https://doi.org/10.1093/cid/cix1125
  7. Reid G. 2016. Probiotics: definition, scope and mechanisms of action. Best Pract. Res. Clin. Gastroenterol. 30: 17-25. https://doi.org/10.1016/j.bpg.2015.12.001
  8. Maldonado Galdeano C, Cazorla SI, Lemme Dumit JM, Velez E, Perdigon G. 2019. Beneficial effects of probiotic consumption on the immune system. Ann. Nutr. Metab. 74: 115-124. https://doi.org/10.1159/000496426
  9. Nomoto K. 2005. Prevention of infections by probiotics. J. Biosci. Bioeng. 100: 583-592. https://doi.org/10.1263/jbb.100.583
  10. Goderska K, Agudo Pena S, Alarcon T. 2018. Helicobacter pylori treatment: antibiotics or probiotics. Appl. Microbiol. Biotechnol. 102: 1-7. https://doi.org/10.1007/s00253-017-8535-7
  11. Gut AM, Vasiljevic T, Yeager T, Donkor ON. 2018. Salmonella infection - prevention and treatment by antibiotics and probiotic yeasts: a review. Microbiology (Reading) 164: 1327-1344. https://doi.org/10.1099/mic.0.000709
  12. Shenoy A, Gottlieb A. 2019. Probiotics for oral and vulvovaginal candidiasis: a review. Dermatol. Ther. 32: e12970. https://doi.org/10.1111/dth.12970
  13. Sihra N, Goodman A, Zakri R, Sahai A, Malde S. 2018. Nonantibiotic prevention and management of recurrent urinary tract infection. Nat. Rev. Urol. 15: 750-776. https://doi.org/10.1038/s41585-018-0106-x
  14. Mills JP, Rao K, Young VB. 2018. Probiotics for prevention of Clostridium difficile infection. Curr. Opin. Gastroenterol. 34: 3-10. https://doi.org/10.1097/MOG.0000000000000410
  15. Wong SS, Quan Toh Z, Dunne EM, Mulholland EK, Tang ML, Robins-Browne RM, et al. 2013. Inhibition of Streptococcus pneumoniae adherence to human epithelial cells in vitro by the probiotic Lactobacillus rhamnosus GG. BMC Res. Notes 6: 135. https://doi.org/10.1186/1756-0500-6-135
  16. Sorokulova IB, Kirik DL, Pinchuk II. 1997. Probiotics against Campylobacter pathogens. J. Travel Med. 4: 167-170. https://doi.org/10.1111/j.1708-8305.1997.tb00813.x
  17. Pamer EG. 2016. Resurrecting the intestinal microbiota to combat antibiotic-resistant pathogens. Science 352: 535-538. https://doi.org/10.1126/science.aad9382
  18. Manley KJ, Fraenkel MB, Mayall BC, Power DA. 2007. Probiotic treatment of vancomycin-resistant enterococci: a randomised controlled trial. Med. J. Aust. 186: 454-457. https://doi.org/10.5694/j.1326-5377.2007.tb00995.x
  19. Karska-Wysocki B, Bazo M, Smoragiewicz W. 2010. Antibacterial activity of Lactobacillus acidophilus and Lactobacillus casei against methicillin-resistant Staphylococcus aureus (MRSA). Microbiol. Res. 165: 674-686. https://doi.org/10.1016/j.micres.2009.11.008
  20. Chen CC, Lai CC, Huang HL, Huang WY, Toh HS, Weng TC, et al. 2019. Antimicrobial activity of Lactobacillus species against carbapenem-resistant enterobacteriaceae. Front. Microbiol. 10: 789. https://doi.org/10.3389/fmicb.2019.00789
  21. Nagasaki A, Takahashi H, Iinuma M, Uchiyama T, Watanabe S, Koide T, et al. 2010. Ulcerative colitis with multidrug-resistant Pseudomonas aeruginosa infection successfully treated with bifidobacterium. Digestion 81: 204-205. https://doi.org/10.1159/000236042
  22. Reikvam DH, Meyer-Myklestad MH, Troseid M, Stiksrud B. 2020. Probiotics to manage inflammation in HIV infection. Curr. Opin. Infect. Dis. 33: 34-43. https://doi.org/10.1097/qco.0000000000000612
  23. Manna S, Chowdhury T, Chakraborty R, Mandal SM. 2021. Probiotics-derived peptides and their immunomodulatory molecules can play a preventive role against viral diseases including COVID-19. Probiotics Antimicrb. Proteins 13: 611-623. https://doi.org/10.1007/s12602-020-09727-7
  24. Kim S, Seo H, Mahmud HA, Islam MI, Kim YS, Lyu J, et al. 2017. In vitro effect of DFC-2 on mycolic acid biosynthesis in Mycobacterium tuberculosis. J. Microbiol. Biotechnol. 27: 1932-1941. https://doi.org/10.4014/jmb.1705.05013
  25. Van Hoecke L, Job ER, Saelens X, Roose K. 2017. Bronchoalveolar lavage of murine lungs to analyze inflammatory cell infiltration. J. Vis. Exp. 4: 55398.
  26. Zerin T, Lee M, Jang WS, Nam KW, Song HY. 2015. Ursolic acid reduces Mycobacterium tuberculosis-induced nitric oxide release in human alveolar A549 cells. Mol. Cells 38: 610-615. https://doi.org/10.14348/MOLCELLS.2015.2328
  27. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119. https://doi.org/10.1186/1471-2105-11-119
  28. Lowe TM, Eddy SR. 1997. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964. https://doi.org/10.1093/nar/25.5.955
  29. Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, et al. 2015. Rfam 12.0: updates to the RNA families database. Nucleic Acids Res. 43: D130-D137. https://doi.org/10.1093/nar/gku1063
  30. Yoon SH, Ha SM, Lim J, Kwon S, Chun J. 2017. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110: 1281-1286. https://doi.org/10.1007/s10482-017-0844-4
  31. Nguyen L. 2016. Antibiotic resistance mechanisms in M. tuberculosis: an update. Arch. Toxicol. 90: 1585-1604. https://doi.org/10.1007/s00204-016-1727-6
  32. Sharma D, Sharma S, Sharma J. 2020. Potential strategies for the management of drug-resistant tuberculosis. J. Glob. Antimicrob. Resist. 22: 210-214. https://doi.org/10.1016/j.jgar.2020.02.029
  33. Liu Y, Wang J, Wu C. 2021. Microbiota and Tuberculosis: a potential role of probiotics, and postbiotics. Front. Nutr. 8: 626254. https://doi.org/10.3389/fnut.2021.626254
  34. Mincheol Kim, JS Chun. 2014. Chapter 4 - 16S rRNA Gene-Based Identification of Bacteria and Archaea using the EzTaxon server. Methods Microbiol. 41: 61-74. https://doi.org/10.1016/bs.mim.2014.08.001
  35. Aubin GG, Bemer P, Kambarev S, Patel NB, Lemenand O, Caillon J, et al. 2016. Propionibacteriumnamnetense sp. nov., isolated from a human bone infection. Int. J. Syst. Evol. Microbiol. 66: 3393-3399. https://doi.org/10.1099/ijsem.0.001204
  36. Chong VH, Lim KS. 2009. Gastrointestinal tuberculosis. Singapore Med. J. 50: 638-645; quiz 646.
  37. Pieters J. 2008. Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe. 3: 399-407. https://doi.org/10.1016/j.chom.2008.05.006
  38. Pan FG, Zhao YY, Zhu S, Sun CJ, Lei LC, Feng X, et al. 2012. Different transcriptional profiles of RAW264.7 infected with Mycobacterium tuberculosis H37Rv and BCG identified via deep sequencing. PLoS One 7: e51988. https://doi.org/10.1371/journal.pone.0051988
  39. Forget EJ, Menzies D. 2006. Adverse reactions to first-line antituberculosis drugs. Expert Opin. Drug Saf. 5: 231-249.
  40. Prasad R, Singh A, Gupta N. 2019. Adverse drug reactions in tuberculosis and management. Indian J. Tuberc. 66: 520-532. https://doi.org/10.1016/j.ijtb.2019.11.005
  41. Deen B, Diez-Gonzalez F. 2019. Assessment of Pediococcus acidilactici ATCC 8042 as potential Salmonella surrogate for thermal treatments of toasted oats cereal and peanut butter. Food Microbiol. 83: 187-192. https://doi.org/10.1016/j.fm.2019.05.015
  42. Bansal P, Kumar R, Singh J, Dhanda S. 2019. Next generation sequencing, biochemical characterization, metabolic pathway analysis of novel probiotic Pediococcus acidilactici NCDC 252 and it's evolutionary relationship with other lactic acid bacteria. Mol. Biol. Rep. 46: 5883-5895. https://doi.org/10.1007/s11033-019-05022-z
  43. Redman MG, Ward EJ, Phillips RS. 2014. The efficacy and safety of probiotics in people with cancer: a systematic review. Ann. Oncol. 25: 1919-1929. https://doi.org/10.1093/annonc/mdu106
  44. Lange K, Buerger M, Stallmach A, Bruns T. 2016. Effects of antibiotics on gut microbiota. Dig. Dis. 34: 260-268. https://doi.org/10.1159/000443360
  45. Iizumi T, Battaglia T, Ruiz V, Perez Perez GI. 2017. Gut microbiome and antibiotics. Arch. Med. Res. 48: 727-734. https://doi.org/10.1016/j.arcmed.2017.11.004
  46. Romanowski K, Balshaw RF, Benedetti A, Campbell JR, Menzies D, Ahmad Khan F, et al. 2019. Predicting tuberculosis relapse in patients treated with the standard 6-month regimen: an individual patient data meta-analysis. Thorax 74: 291-297. https://doi.org/10.1136/thoraxjnl-2017-211120
  47. Lange C, Dheda K, Chesov D, Mandalakas AM, Udwadia Z, Horsburgh CR, Jr. 2019. Management of drug-resistant tuberculosis. Lancet 394: 953-966. https://doi.org/10.1016/s0140-6736(19)31882-3
  48. O'Toole RF, Gautam SS. 2018. The host microbiome and impact of tuberculosis chemotherapy. Tuberculosis (Edinb) 113: 26-29. https://doi.org/10.1016/j.tube.2018.08.015
  49. Hong BY, Maulen NP, Adami AJ, Granados H, Balcells ME, Cervantes J. 2016. Microbiome changes during tuberculosis and antituberculous therapy. Clin. Microbiol. Rev. 29: 915-926. https://doi.org/10.1128/CMR.00096-15
  50. Eslami M, Bahar A, Keikha M, Karbalaei M, Kobyliak NM, Yousefi B. 2020. Probiotics function and modulation of the immune system in allergic diseases. Allergol. Immunopathol. (Madr). 48: 771-788. https://doi.org/10.1016/j.aller.2020.04.005
  51. Bogdan C. 2001. Nitric oxide and the immune response. Nat. Immunol. 2: 907-916. https://doi.org/10.1038/ni1001-907
  52. Chakravortty D, Hensel M. 2003. Inducible nitric oxide synthase and control of intracellular bacterial pathogens. Microbes Infect. 5: 621-627. https://doi.org/10.1016/S1286-4579(03)00096-0
  53. Suprapti B, Suharjono S, Raising R, Yulistiani Y, Izzah Z, Nilamsari WP, et al. 2018. Effects of probiotics and Vitamin B supplementation on IFN-gamma and IL-12 levels during intensive phase treatment of tuberculosis. Indones J. Pharm. 29: 80-85. https://doi.org/10.14499/indonesianjpharm29iss2pp80