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Comparison of probiotic Lactobacillus strains isolated from dairy and Iranian traditional food products with those from human source on intestinal microbiota using BALB/C mice model

  • Food Microbiology - Research Paper
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Abstract

This study compares the probiotic Lactobacillus strains isolated from dairy and Iranian traditional food products with those from human sources on intestinal microbiota using BALB/C mice model. First, Lactiplantibacillus plantarum (M11), Limosilactobacillus fermentum (19SH), Lactobacillus acidophilus (AC2), and Lactobacillus gasseri (52b) strains, isolated from either Iranian traditionally fermented products or human (healthy woman vaginal secretions), identified with molecular methods and selected based on the surface hydrophobicity, auto- and co-aggregation, were investigated for their probiotic properties and compared with their standard probiotic strains in vitro. The native strains and their mixtures (MIX) were then orally fed to five groups of female inbred BALB/C mice over the course of 38 days by gavage at 0.5 and 4 McFarland, respectively, equal to 1.5 × 108 and 1 × 109 cfu/ml. Feeding paused for 6 days to test the bacteria’s adhesion in vivo. According to the findings, the probiotic Lactobacillus strain isolated from human source (52b) exhibited the best in vitro and in vivo adhesion ability. Probiotic Lactobacillus strains isolated from Iranian traditional food products (19SH and AC2) had the most co-aggregation with Listeria monocytogenes (ATTC 7644), Salmonella enterica subsp. enterica (ATCC 13,076), and Escherichia coli (NCTC 12,900 O157:H7) in vitro. These strains produced the most profound decreasing effect on the mice intestinal microbiota and pathogens in vivo. The difference in the strains and their probiotic potential is related to the sources from which they are isolated as well as their cell walls. The results suggest that (19SH and 52b strains) are the best candidates to investigate the cell wall and its effect on the host immune system.

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References

  1. Hill GB, Eschenbach DA, Holmes KK (1984) Bacteriology of the vagina. Scand J urol Nephrol Suppl 86:23–39. https://doi.org/10.1371/journal.pbio.3000788

    Article  CAS  PubMed  Google Scholar 

  2. Servin AL (2004) Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28(4):405–440. https://doi.org/10.1016/j.femsre.2004.01.003

    Article  CAS  PubMed  Google Scholar 

  3. Hernández-González JC, Martínez-Tapia A, Lazcano-Hernández G, García-Pérez BE, Castrejón-Jiménez NS (2021) Bacteriocins from lactic acid bacteria a powerful alternative as antimicrobials, probiotics, and immunomodulators in veterinary medicine. Animals 11(4):979. https://doi.org/10.3390/ani11040979

    Article  PubMed  PubMed Central  Google Scholar 

  4. Zommiti M, Feuilloley MG, Connil N (2020) Update of probiotics in human world: a nonstop source of benefactions till the end of time. Microorganisms 8:1907–1940. https://doi.org/10.3390/microorganisms8121907

    Article  CAS  PubMed Central  Google Scholar 

  5. Markowiak P, Śliżewska K (2017) Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9(9):1021–1051. https://doi.org/10.3390/nu9091021

    Article  CAS  PubMed Central  Google Scholar 

  6. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Berni canani R, Flint H, Salminen S, Calder PhC, Sanders ME, (2014) Expert consensus document: the International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506–514. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  7. Salminen S, Nybom S, Meriluoto J, Collado MC, Vesterlund S, El-Nezami H (2010) Interaction of probiotics and pathogens benefits to human health? Curr Opin Biotechnol 21(2):157–167. https://doi.org/10.1016/j.copbio.2010.03.016

    Article  CAS  PubMed  Google Scholar 

  8. DeWaard R, Garssen J, Bokken GCAM, Vos JG (2002) Antagonistic activity of Lactobacillus casei strain Shirota against gastrointestinal Listeria monocytogenes infection in rats. Int J Food Microbiol 73(1):93–100. https://doi.org/10.1016/S0168-1605(01)00699-7

    Article  CAS  Google Scholar 

  9. Gill HS, Shu Q, Lin H, Rutherfurd KJ, Cross ML (2001) Protection against translocating Salmonella typhimurium infection in mice by feeding the immuno-enhancing probiotic Lactobacillus rhamnosus strain HN001. Med Microbiol Immunolog 190(3):97–104. https://doi.org/10.1007/s004300100095

    Article  CAS  Google Scholar 

  10. Thoreux K, Balas D, Bouley C, Senegas-Balas F (1998) Diet supplemented with yoghurt or milk fermented by Lactobacillus casei DN-114 001 stimulates growth and brush-border enzyme activities in mouse small intestine. Digestion 59(4):349–359. https://doi.org/10.1159/000007514

    Article  CAS  PubMed  Google Scholar 

  11. Shu Q, Gill HS (2001) A dietary probiotic (Bifidobacterium lactis HN019) reduces the severity of Escherichia coli O157:H7 infection in mice. Med Microbiol Immunol 189:147–152. https://doi.org/10.1007/s430-001-8021-9

    Article  CAS  PubMed  Google Scholar 

  12. Rajoka M, Hayat H, Sarwar S, Mehwish H, Ahmad F, Hussain N, Shah SZH, Khurshid M, Siddiqu M, Shi J (2018) Isolation and evaluation of probiotic potential of lactic acid bacteria isolated from poultry intestine. Microbiol 87(1):116–126. https://doi.org/10.1134/S0026261718010150

    Article  CAS  Google Scholar 

  13. Campana R, van Hemert S, Baffone W (2017) Strain-specific probiotic properties of lactic acid bacteria and their interference with human intestinal pathogens invasion. Gut Pathog 9(1):1–12. https://doi.org/10.1186/s13099-017-0162-4

    Article  Google Scholar 

  14. Vasiee A, Alizadeh Behbahani B, Tabatabaei Yazdi F, Mortazavi SA, Noorbakhsh H (2017) Diversity and probiotic potential of lactic acid bacteria isolated from Horreh, a traditional iranian fermented food. Probiotics Antimicrob Proteins 10(2):258–268. https://doi.org/10.1007/s12602-017-9282-x

    Article  CAS  Google Scholar 

  15. Tokatlı M, Gülgör G, Bağder Elmacı S, Arslankoz İşleyen N, Özçelik F (2015) In vitro properties of potential probiotic indigenous lactic acid bacteria originating from traditional pickles. BioMed Res Int 2015:8–16. https://doi.org/10.1155/2015/315819

    Article  CAS  Google Scholar 

  16. Yavuzdurmaz H (2007) Isolation, characterization, determination of probiotic properties of lactic acid bacteria from human milk (Master’s thesis, Izmir Institute of Technology). A Thesis Submitted to the Graduate School of Engineering and Sciences of Izmir Institute of Technology.

  17. Joghataei M, Shahidi F, Pouladfar G, Mortazavi SA, Ghaderi A (2019) Probiotic potential comparison of Lactobacillus strains isolated from Iranian traditional food products and human feces with standard probiotic strains. J Sci Food Agric 99(15):6680–6688. https://doi.org/10.1002/jsfa.9945

    Article  CAS  PubMed  Google Scholar 

  18. Juárez Tomás MS, Wiese B, Nader-Macías ME (2005) Effects of culture conditions on the growth and auto-aggregation ability of vaginal Lactobacillus johnsonii CRL 1294. J Appl Microbiol 99(6):1383–1391. https://doi.org/10.1111/j.1365-2672.2005.02726.x

    Article  CAS  PubMed  Google Scholar 

  19. Panel EF (2012) Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J 10(6):2740–2750. https://doi.org/10.2903/j.efsa.2012.2740

    Article  CAS  Google Scholar 

  20. Klare I, KonstabelMüller-Bertling S, Reissbrodt R, Huys G, Vancanneyt M, Swings J, Goossens H, Witte W, C (2005) Evaluation of new broth media for microdilution antibiotic susceptibility testing of Lactobacilli, Pediococci, Lactococci, and Bifidobacteria. Appl Environ Microbiol 71(12):8982–8986

    Article  CAS  Google Scholar 

  21. Festing MF, Altman DG (2002) Guidelines for the design and statistical analysis of experiments using laboratory animals. ILAR J 43(4): 244–258. http://www.ncbi.nlm.nih.gov/pubmed/12391400

  22. Lang TA, Altman DG (2015) Basic statistical reporting for articles published in biomedical journals the “statistical analyses and methods in the published literature” or the SAMPL Guidelines. Int J Nurs Stud 52(1):5–9. https://doi.org/10.1016/j.ijnurstu.2014.09.006

    Article  PubMed  Google Scholar 

  23. Percie du Sert N, Bamsey I, Bate ST, Berdoy M, Clark RA, Cuthill I et al (2017) The experimental design assistant. PLoS Biol 15(9):e2003779. https://doi.org/10.1371/journal.pbio.2003779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wang S, Ahmadi S, Nagpal R, Jain S, Mishra SP, Kavanagh K et al (2020) Lipoteichoic acid from the cell wall of a heat killed Lactobacillus paracasei D3–5 ameliorates aging-related leaky gut, inflammation and improves physical and cognitive functions: from C elegans to mice. GeroScience 42(1):333–352

    Article  CAS  Google Scholar 

  25. Aindelis G, Tiptiri-Kourpeti A, Lampri E, Spyridopoulou K, Lamprianidou E, Kotsianidis L, Ypsilantis P, Pappa A, Chlichlia K (2020) Immune responses raised in an experimental colon carcinoma model following oral administration of Lactobacillus casei. Cancers 12(2):368. https://doi.org/10.3390/cancers12020368

    Article  CAS  PubMed Central  Google Scholar 

  26. Yazdi MH, Dallal MMS, Hassan ZM, Holakuyee M, Amiri SA, Abolhassani M, Mahdavi M (2010) Oral administration of Lactobacillus acidophilus induces IL-12 production in spleen cell culture of BALB/C mice bearing transplanted breast tumour. Br J Nutr 104(2):227–232. https://doi.org/10.1017/S0007114510000516

    Article  CAS  PubMed  Google Scholar 

  27. Murosaki S, Muroyama K, Yamamoto Y, Yoshikai Y (2000) Antitumor effect of heat-killed Lactobacillus plantarum L-137 through restoration of impaired interleukin-12 production in tumor-bearing mice. Cancer Immunol Immunother 49(3):157–164. https://doi.org/10.1007/s002620050615

    Article  CAS  PubMed  Google Scholar 

  28. 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(1):22–29. https://doi.org/10.1016/j.fm.2013.03.010

    Article  CAS  PubMed  Google Scholar 

  29. Atassi F, Servin AL (2010) Individual and co-operative roles of lactic acid and hydrogen peroxide in the killing activity of enteric strain Lactobacillus johnsonii NCC933 and vaginal strain Lactobacillus gasseri KS120.1 against enteric, uropathogenic and vaginosis-associated pathogens. FEMS Microbiol Lett 304(1):29–38

    Article  CAS  Google Scholar 

  30. Robinson RK (2014) Encyclopedia of food microbiology. Academic press. Carl A (ed). Batt, Pradip Patel, cornell university, Ithaca, NY, USA. ISBN:978–0–12–384730–0

  31. Ryan KJ, Ray CG (2004) Medical microbiology. Mc Graw Hill, New york.

  32. Itoh H, Sashihara T, Hosono A, Kaminogawa S, Uchida M (2011) Interleukin-12 inhibits development of ectopic endometriotic tissues in peritoneal cavity via activation of NK cells in a murine endometriosis model. Cytotechnology 63(2):133–141. https://doi.org/10.1007/s10616-010-9321-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Mirlohi M, Soleymanianzad S, Dokhani SH, Sheykh ZAM, Abghari A (2009) Investigation of acid and bile tolerance of native lactobacilli isolated from fecal samples and commercial probiotics by growth and survival studies. Iran J Biotechnol 7(4): 233–240. https://www.sid.ir/en/journal/ViewPaper.aspx?id=163393

  34. Frece J, Kos B, Svetec IK, Zgaga Z, Mrša V, Šušković J (2005) Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92. J Appl Microbiol 98(2):285–292. https://doi.org/10.1111/j.1365-2672.2004.02473.x

    Article  CAS  PubMed  Google Scholar 

  35. Rushdy AA, Gomaa EZ (2013) Antimicrobial compounds produced by probiotic Lactobacillus brevis isolated from dairy products. Ann Microbiol 98(2):285–292. https://doi.org/10.1007/s13213-012-0447-2

    Article  CAS  Google Scholar 

  36. Barinov A, Bolotin A, Langella P, Maguin E, Van De Guchte M (2011) Lactic Acid Bacteria and Bifidobacteria. Caister Academic Press, U.K.

    Google Scholar 

  37. Nishiyama K, Sugiyama M, Mukai T (2016) Adhesion properties of lactic acid bacteria on intestinal mucin. Microorganisms 4(3):34–52. https://doi.org/10.3390/microorganisms4030034

    Article  CAS  PubMed Central  Google Scholar 

  38. Mater DD, Langella P, Corthier G, Flores MJ (2008) A probiotic Lactobacillus strain can acquire vancomycin resistance during digestive transit in mice. J Mol Microbio Biotechnol 14(1–3):123–127

    CAS  Google Scholar 

  39. Tomaro-Duchesneau C, Jones ML, Shah D, Jain P, Saha S, Prakash S (2014) Cholesterol assimilation by Lactobacillus probiotic bacteria: an in vitro investigation. BioMed Res Int 2014:1–9

    Article  Google Scholar 

  40. Lebeer S, Vanderleyden J, De Keersmaecker SC (2008) Genes and molecules of lactobacilli supporting probiotic action. M M B R J 72(4):728–764. https://doi.org/10.1128/MMBR.00017-08

    Article  CAS  Google Scholar 

  41. Desvaux M, Dumas E, Chafsey I, Hebraud M (2006) Protein cell surface display in Gram-positive bacteria: from single protein to macromolecular protein structure. FEMS Microbiol Lett 256(1):1–15

    Article  CAS  Google Scholar 

  42. Shiraishi T, Yokota SI, Morita N, Fukiya S, Tomita S, Tanaka N, Okada S, Yokota A (2013) Characterization of a Lactobacillus gasseri JCM 1131T lipoteichoic acid with a novel glycolipid anchor structure. Appl Environ Microbiol 79(10):3315–3318. https://doi.org/10.1128/AEM.00243-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Cotter PD, Ross RP, Hill C (2013) Bacteriocins a viable alternative to antibiotics? Nat Rev Microbiol 11(2):95–105. https://doi.org/10.1038/nrmicro2937

    Article  CAS  PubMed  Google Scholar 

  44. Ogunbanwo S, Sanni A, Onilude A (2004) Influence of bacteriocin in the control of Escherichia coli infection of broiler chickens in Nigeria. World J Microbiol Biotechnol 20:51–56

    Article  CAS  Google Scholar 

  45. Wang Q, Cui Y, Wang W, Xu J, Xu L (2012) Production of two bacteriocins in various growth conditions produced by gram-positive bacteria isolated from chicken cecum. Can J Microbiol 58(1):93–101. https://doi.org/10.1139/w11-108

    Article  CAS  PubMed  Google Scholar 

  46. Kahouli I, Malhotra M, Alaoui-Jamali M, Prakash S (2015) In-vitro characterization of the anti-cancer activity of the probiotic bacterium Lactobacillus fermentum NCIMB 5221 and potential against colorectal cancer. J Cancer Sci Ther 7(7):224–235. https://doi.org/10.4172/1948-5956.1000354

    Article  CAS  Google Scholar 

  47. Wang Y, Corrieu G, Béal C (2005) Fermentation pH and temperature influence the cryotolerance of Lactobacillus acidophilus RD758. J Dairy Sci 88(1):21–29. https://doi.org/10.3168/jds.S0022-0302(05)72658-8

    Article  CAS  PubMed  Google Scholar 

  48. Macfarlane GT, Macfarlane S (2012) Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int 95(1):50–60. https://doi.org/10.5740/jaoacint.SGE_Macfarlane

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge the Bu-Ali Research Institute, Immunology Research Center, Mashhad University of medical sciences, Iran, as well as the technical assistance offered by the Molecular Genetics and Novel Technologies Laboratory at the Department of Food Science and Technology, Faculty of Agriculture, Ferdowsi University of Mashhad, Iran.

Funding

This work was supported by a grant (No. 3.51765) from by the research deputy of Ferdowsi University of Mashhad, Iran.

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Conceptualization: Samaneh Hatami, Masoud Yavarmanesh. Methodology: Masoud Yavarmanesh, Mojtaba Sankian, Samaneh Hatami. Formal analysis and investigation: Samaneh Hatami. Writing—original draft preparation: Samaneh Hatami, Seyed Ali Issazadeh. Writing—review and editing: Samaneh Hatami, Masoud Yavarmanesh. Resources: Samaneh Hatami, Seyed Ali Issazadeh. Supervision: Masoud Yavarmanesh, Mojtaba Sankian. Software: Samaneh Hatami, Seyed Ali Issazadeh. Project administration: Masoud Yavarmanesh. All authors approved final version submitted.

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Correspondence to Masoud Yavarmanesh.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This study involves animal testing (mice). The ethical criteria with the code of IR.UM.REC.1400.004 (Ferdowsi University of Mashhad, Iran) were observed.

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Hatami, S., Yavarmanesh, M., Sankian, M. et al. Comparison of probiotic Lactobacillus strains isolated from dairy and Iranian traditional food products with those from human source on intestinal microbiota using BALB/C mice model. Braz J Microbiol 53, 1577–1591 (2022). https://doi.org/10.1007/s42770-022-00790-6

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