Advertisement

Probiotics and Antimicrobial Proteins

, Volume 11, Issue 3, pp 887–904 | Cite as

Probiotics L. acidophilus and B. clausii Modulate Gut Microbiota in Th1- and Th2-Biased Mice to Ameliorate Salmonella Typhimurium-Induced Diarrhea

  • Biswaranjan Pradhan
  • Dipanjan Guha
  • Aman Kumar Naik
  • Arka Banerjee
  • Subodh Tambat
  • Saurabh Chawla
  • Shantibhusan Senapati
  • Palok AichEmail author
Article

Abstract

Gut microbiota play important role in maintaining health. Probiotics are believed to augment it further. We aimed at comparing effects of probiotics, Lactobacillus acidophilus (LA) and Bacillus clausii (BC) (a) on the gut microbiota abundance and diversity and (b) their contributions to control intestinal dysbiosis and inflammation in Th1- and Th2-biased mice following Salmonella infection. We report how could gut microbiota and the differential immune bias (Th1 or Th2) of the host regulate host responses when challenged with Salmonella typhimurium in the presence and absence of either of the probiotics. LA was found to be effective in ameliorating the microbial dysbiosis and inflammation caused by Salmonella infection, in Th1 (C57BL/6) and Th2 (BALB/c)-biased mouse. BC was able to ameliorate Salmonella-induced dysbiosis and inflammation in Th2 but not in Th1-biased mouse. These results may support probiotics LA as a treatment option in the case of Salmonella infection.

Keywords

Probiotics Microbiota Dysbiosis Inflammation Lactobacillus Salmonella 

Notes

Acknowledgments

We acknowledge and we are thankful to Mr. Madan Mohan Mallick and Mr. Susanta Kumar Swain, the technicians of Dr. Shantibhusan Senapati’s laboratory for making the histological slides. We deeply appreciate Bionivid, Xcelris Lab and SciGenome for timely execution of 16S rRNA sequencing. We acknowledge Mr. Sibabrata Sarangi, attendant, NISER animal house for taking care of the animals during the experiments. We heartily appreciate Mr. David Alexander Datzkiw for proofreading this manuscript.

Data Submission

The transcriptomics data discussed in this publication have been deposited in NCBI’s Gene Expression Omnibus and are accessible through GEO series accession number GSE98353 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?token=excdimugvlubnkj&acc=GSE98353).

The 16S rDNA sequencing data discussed in this publication have been deposited in NCBI’s Sequence Read Archive and are accessible through Bio project number PRJNA388784 (http://www.ncbi.nlm.nih.gov/bioproject/388784) and PRJNA392028 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA392028).

Author Contributions

P.A. and B.P. planned the study and designed the experiments. B.P. executed most of the experiments and D.G., A.K.N, A.B. assisted in the experiments with supervision from P.A., S.S., S.C., B.P., and D.G. analyzed the histopathological data. P.A., B.P., and D.G. analyzed the microarray data. S.T., B.P., P.A., and A.B. analyzed the microbiome data. BP prepared the first draft of the manuscript. P.A. overall supervised the work and finalized the manuscript.

Funding Information

This study is provided by the Department of Biotechnology (DBT), Government of India for partially funding this project through extramural support. The funders had no role in study design, data collection, and interpretation, or the decision to submit the work for publication

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest with the contents of this article.

Supplementary material

12602_2018_9436_MOESM1_ESM.docx (51.5 mb)
ESM 1 (DOCX 52784 kb)

References

  1. 1.
    Marchesi JR, Adams DH, Fava F, Hermes GD, Hirschfield GM, Hold G, Quraishi MN, Kinross J, Smidt H, Tuohy KM, Thomas LV, Zoetendal EG, Hart A (2016) The gut microbiota and host health: a new clinical frontier. Gut 65(2):330–339.  https://doi.org/10.1136/gutjnl-2015-309990 Google Scholar
  2. 2.
    Moelling K (2016) Nutrition and the microbiome. Ann N Y Acad Sci 1372(1):3–8.  https://doi.org/10.1111/nyas.13039 Google Scholar
  3. 3.
    Smoot DT, Mobley HLT, Chippendale GR, Lewison JF, Resau JH (1990) Helicobacter pylori urease activity is toxic to human gastric epithelial-cells. Infect Immun 58(6):1992–1994Google Scholar
  4. 4.
    Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, Russell JM, Bevins CL, Adams LG, Tsolis RM, Roth JR, Baumler AJ (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467(7314):426–429.  https://doi.org/10.1038/nature09415 Google Scholar
  5. 5.
    Huurre A, Kalliomäki M, Rautava S, Rinne M, Salminen S, Isolauri E (2007) Mode of delivery—effects on gut microbiota and humoral immunity. Neonatology 93(4):236–240Google Scholar
  6. 6.
    Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI (2012) Human gut microbiome viewed across age and geography. Nature 486(7402):222–227.  https://doi.org/10.1038/nature11053 Google Scholar
  7. 7.
    Modi SR, Collins JJ, Relman DA (2014) Antibiotics and the gut microbiota. J Clin Invest 124(10):4212–4218.  https://doi.org/10.1172/JCI72333 Google Scholar
  8. 8.
    Schultz BM, Paduro CA, Salazar GA, Salazar-Echegarai FJ, Sebastian VP, Riedel CA, Kalergis AM, Alvarez-Lobos M, Bueno SM (2017) A potential role of Salmonella infection in the onset of inflammatory bowel diseases. Front Immunol 8:191.  https://doi.org/10.3389/fimmu.2017.00191 Google Scholar
  9. 9.
    Everard A, Cani PD (2013) Diabetes, obesity and gut microbiota. Best Pract Res Clin Gastroenterol 27(1):73–83.  https://doi.org/10.1016/j.bpg.2013.03.007 Google Scholar
  10. 10.
    Louis P, Hold GL, Flint HJ (2014) The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 12(10):661–672.  https://doi.org/10.1038/nrmicro3344 Google Scholar
  11. 11.
    Hold GL, Smith M, Grange C, Watt ER, El-Omar EM, Mukhopadhya I (2014) Role of the gut microbiota in inflammatory bowel disease pathogenesis: what have we learnt in the past 10 years? World J Gastroentero 20(5):1192–1210.  https://doi.org/10.3748/wjg.v20.i5.1192 Google Scholar
  12. 12.
    Alzahrani S, Lina TT, Gonzalez J, Pinchuk IV, Beswick EJ, Reyes VE (2014) Effect of Helicobacter pylori on gastric epithelial cells. World J Gastroenterol 20(36):12767–12780.  https://doi.org/10.3748/wjg.v20.i36.12767 Google Scholar
  13. 13.
    Patel S, McCormick BA (2014) Mucosal inflammatory response to Salmonella typhimurium infection. Front Immunol 5:311.  https://doi.org/10.3389/fimmu.2014.00311 Google Scholar
  14. 14.
    Wotzka SY, Nguyen BD, Hardt WD (2017) Salmonella typhimurium diarrhea reveals basic principles of enteropathogen infection and disease-promoted DNA exchange. Cell Host Microbe 21(4):443–454.  https://doi.org/10.1016/j.chom.2017.03.009 Google Scholar
  15. 15.
    Cario E (2008) Innate immune signalling at intestinal mucosal surfaces: a fine line between host protection and destruction. Curr Opin Gastroenterol 24(6):725–732.  https://doi.org/10.1097/MOG.0b013e32830c4341 Google Scholar
  16. 16.
    Servin AL, Coconnier MH (2003) Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract Res Clin Gastroenterol 17(5):741–754Google Scholar
  17. 17.
    Wells JM, Rossi O, Meijerink M, van Baarlen P (2010) Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci 108(Supplement 1):4607–4614.  https://doi.org/10.1073/pnas.1000092107 Google Scholar
  18. 18.
    Pradhan B, Guha D, Ray P, Das D, Aich P (2016) Comparative analysis of the effects of two probiotic bacterial strains on metabolism and innate immunity in the RAW 264.7 murine macrophage cell line. Probiotics Antimicrob Proteins 8(2):73–84.  https://doi.org/10.1007/s12602-016-9211-4 Google Scholar
  19. 19.
    Moore RJ, Stanley D (2016) Experimental design considerations in microbiota/inflammation studies. Clin Transl Immunology 5(7):e92.  https://doi.org/10.1038/cti.2016.41 Google Scholar
  20. 20.
    Sur A, Pradhan B, Banerjee A, Aich P (2015) Immune activation efficacy of indolicidin is enhanced upon conjugation with carbon nanotubes and gold nanoparticles. PLoS One 10(4):e0123905Google Scholar
  21. 21.
    Hokamp K, Roche FM, Acab M, Rousseau ME, Kuo B, Goode D, Aeschliman D, Bryan J, Babiuk LA, Hancock RE, Brinkman FS (2004) ArrayPipe: a flexible processing pipeline for microarray data. Nucleic Acids Res 32(Web Server):W457–W459.  https://doi.org/10.1093/nar/gkh446 Google Scholar
  22. 22.
    Zhang B, Kirov S, Snoddy J (2005) WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res 33(suppl 2):W741–W748.  https://doi.org/10.1093/nar/gki475 Google Scholar
  23. 23.
    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998.  https://doi.org/10.1038/nmeth.2604 Google Scholar
  24. 24.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336.  https://doi.org/10.1038/nmeth.f.303 Google Scholar
  25. 25.
    Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. Bmc Bioinformatics 9(1):1Google Scholar
  26. 26.
    Arndt D, Xia J, Liu Y, Zhou Y, Guo AC, Cruz JA, Sinelnikov I, Budwill K, Nesbo CL, Wishart DS (2012) METAGENassist: a comprehensive web server for comparative metagenomics. Nucleic Acids Res 40(Web Server issue):W88–W95.  https://doi.org/10.1093/nar/gks497 Google Scholar
  27. 27.
    de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20(9):1453–1454.  https://doi.org/10.1093/bioinformatics/bth078 Google Scholar
  28. 28.
    Saldanha AJ (2004) Java Treeview—extensible visualization of microarray data. Bioinformatics 20(17):3246–3248.  https://doi.org/10.1093/bioinformatics/bth349 Google Scholar
  29. 29.
    Huson DH, Weber N (2013) Microbial community analysis using MEGAN. Methods Enzymol 531:465–485.  https://doi.org/10.1016/B978-0-12-407863-5.00021-6 Google Scholar
  30. 30.
    Colwell RK, Elsensohn JE (2014) EstimateS turns 20: statistical estimation of species richness and shared species from samples, with non-parametric extrapolation. Ecography 37(6):609–613.  https://doi.org/10.1111/ecog.00814 Google Scholar
  31. 31.
    Menke S, Gillingham MA, Wilhelm K, Sommer S (2017) Home-made cost effective preservation buffer is a better alternative to commercial preservation methods for microbiome research. Front Microbiol 8:102.  https://doi.org/10.3389/fmicb.2017.00102 Google Scholar
  32. 32.
    Roth S, Franken P, Sacchetti A, Kremer A, Anderson K, Sansom O, Fodde R (2012) Paneth cells in intestinal homeostasis and tissue injury. PLoS One 7(6):e38965.  https://doi.org/10.1371/journal.pone.0038965 Google Scholar
  33. 33.
    Jin W, Dong C (2013) IL-17 cytokines in immunity and inflammation. Emerg Microbes Infect 2(9):e60.  https://doi.org/10.1038/emi.2013.58 Google Scholar
  34. 34.
    Mayuzumi H, Inagaki-Ohara K, Uyttenhove C, Okamoto Y, Matsuzaki G (2010) Interleukin-17A is required to suppress invasion of Salmonella enterica serovar Typhimurium to enteric mucosa. Immunology 131(3):377–385.  https://doi.org/10.1111/j.1365-2567.2010.03310.x Google Scholar
  35. 35.
    Dicksved J, Halfvarson J, Rosenquist M, Jarnerot G, Tysk C, Apajalahti J, Engstrand L, Jansson JK (2008) Molecular analysis of the gut microbiota of identical twins with Crohn’s disease. ISME J 2(7):716–727.  https://doi.org/10.1038/ismej.2008.37 Google Scholar
  36. 36.
    Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 104(34):13780–13785.  https://doi.org/10.1073/pnas.0706625104 Google Scholar
  37. 37.
    Carroll IM, Ringel-Kulka T, Keku TO, Chang YH, Packey CD, Sartor RB, Ringel Y (2011) Molecular analysis of the luminal- and mucosal-associated intestinal microbiota in diarrhea-predominant irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 301(5):G799–G807.  https://doi.org/10.1152/ajpgi.00154.2011 Google Scholar
  38. 38.
    Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, Young VB (2008) Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 197(3):435–438.  https://doi.org/10.1086/525047 Google Scholar
  39. 39.
    Young VB, Schmidt TM (2004) Antibiotic-associated diarrhea accompanied by large-scale alterations in the composition of the fecal microbiota. J Clin Microbiol 42(3):1203–1206Google Scholar
  40. 40.
    Fransen F, Zagato E, Mazzini E, Fosso B, Manzari C, El Aidy S, Chiavelli A, D'Erchia AM, Sethi MK, Pabst O, Marzano M, Moretti S, Romani L, Penna G, Pesole G, Rescigno M (2015) BALB/c and C57BL/6 mice differ in polyreactive IgA abundance, which impacts the generation of antigen-specific IgA and microbiota diversity. Immunity 43(3):527–540.  https://doi.org/10.1016/j.immuni.2015.08.011 Google Scholar
  41. 41.
    Rooks MG, Garrett WS (2016) Gut microbiota, metabolites and host immunity. Nat Rev Immunol 16(6):341–352.  https://doi.org/10.1038/nri.2016.42 Google Scholar
  42. 42.
    Usami M, Kishimoto K, Ohata A, Miyoshi M, Aoyama M, Fueda Y, Kotani J (2008) Butyrate and trichostatin A attenuate nuclear factor kappaB activation and tumor necrosis factor alpha secretion and increase prostaglandin E2 secretion in human peripheral blood mononuclear cells. Nutr Res 28(5):321–328.  https://doi.org/10.1016/j.nutres.2008.02.012 Google Scholar
  43. 43.
    Vinolo MA, Rodrigues HG, Hatanaka E, Sato FT, Sampaio SC, Curi R (2011) Suppressive effect of short-chain fatty acids on production of proinflammatory mediators by neutrophils. J Nutr Biochem 22(9):849–855.  https://doi.org/10.1016/j.jnutbio.2010.07.009 Google Scholar
  44. 44.
    Bloes DA, Kretschmer D, Peschel A (2015) Enemy attraction: bacterial agonists for leukocyte chemotaxis receptors. Nat Rev Microbiol 13(2):95–104.  https://doi.org/10.1038/nrmicro3390 Google Scholar
  45. 45.
    Willemsen LEM, Koetsier MA, Van Deventer SJH, Van Tol EAF (2003) Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E1 and E2 production by intestinal myofibroblasts. Gut 52(10):1442–1447Google Scholar
  46. 46.
    Gaudier E, Jarry A, Blottiere HM, de Coppet P, Buisine MP, Aubert JP, Laboisse C, Cherbut C, Hoebler C (2004) Butyrate specifically modulates MUC gene expression in intestinal epithelial goblet cells deprived of glucose. Am J Physiol Gastrointest Liver Physiol 287(6):G1168–G1174.  https://doi.org/10.1152/ajpgi.00219.2004 Google Scholar
  47. 47.
    Chen J, Rao JN, Zou T, Liu L, Marasa BS, Xiao L, Zeng X, Turner DJ, Wang JY (2007) Polyamines are required for expression of Toll-like receptor 2 modulating intestinal epithelial barrier integrity. Am J Physiol Gastrointest Liver Physiol 293(3):G568–G576.  https://doi.org/10.1152/ajpgi.00201.2007 Google Scholar
  48. 48.
    Liu L, Guo X, Rao JN, Zou TT, Xiao L, Yu TX, Timmons JA, Turner DJ, Wang JY (2009) Polyamines regulate E-cadherin transcription through c-Myc modulating intestinal epithelial barrier function. Am J Phys Cell Phys 296(4):C801–C810.  https://doi.org/10.1152/ajpcell.00620.2008 Google Scholar
  49. 49.
    Duc le H, Hong HA, Barbosa TM, Henriques AO, Cutting SM (2004) Characterization of Bacillus probiotics available for human use. Appl Environ Microbiol 70(4):2161–2171Google Scholar
  50. 50.
    Huang IF, Lin IC, Liu PF, Cheng MF, Liu YC, Hsieh YD, Chen JJ, Chen CL, Chang HW, Shu CW (2015) Lactobacillus acidophilus attenuates Salmonella-induced intestinal inflammation via TGF-beta signaling. BMC Microbiol 15:203.  https://doi.org/10.1186/s12866-015-0546-x Google Scholar
  51. 51.
    Maroof H, Hassan ZM, Mobarez AM, Mohamadabadi MA (2012) Lactobacillus acidophilus could modulate the immune response against breast cancer in murine model. J Clin Immunol 32(6):1353–1359.  https://doi.org/10.1007/s10875-012-9708-x Google Scholar
  52. 52.
    Marseglia GL, Tosca M, Cirillo I, Licari A, Leone M, Marseglia A, Castellazzi AM, Ciprandi G (2007) Efficacy of Bacillus clausii spores in the prevention of recurrent respiratory infections in children: a pilot study. Ther Clin Risk Manag 3(1):13–17Google Scholar
  53. 53.
    Perdigon G, Maldonado Galdeano C, Valdez JC, Medici M (2002) Interaction of lactic acid bacteria with the gut immune system. Eur J Clin Nutr 56(Suppl 4):S21–S26.  https://doi.org/10.1038/sj.ejcn.1601658 Google Scholar
  54. 54.
    Ripert G, Racedo SM, Elie AM, Jacquot C, Bressollier P, Urdaci MC (2016) Secreted compounds of the probiotic Bacillus clausii strain O/C inhibit the cytotoxic effects induced by Clostridium difficile and Bacillus cereus toxins. Antimicrob Agents Chemother 60(6):3445–3454.  https://doi.org/10.1128/AAC.02815-15 Google Scholar
  55. 55.
    Weiss G, Rasmussen S, Zeuthen LH, Nielsen BN, Jarmer H, Jespersen L, Frokiaer H (2010) Lactobacillus acidophilus induces virus immune defence genes in murine dendritic cells by a Toll-like receptor-2-dependent mechanism. Immunology 131(2):268–281.  https://doi.org/10.1111/j.1365-2567.2010.03301.x Google Scholar
  56. 56.
    Yan F, Polk DB (2011) Probiotics and immune health. Curr Opin Gastroenterol 27(6):496–501.  https://doi.org/10.1097/MOG.0b013e32834baa4d Google Scholar
  57. 57.
    Menconi A, Morgan MJ, Pumford NR, Hargis BM, Tellez G (2013) Physiological properties and Salmonella growth inhibition of probiotic Bacillus strains isolated from environmental and poultry sources. Int J Bacteriol 2013:958408. doi: https://doi.org/10.1155/2013/958408, 1, 8
  58. 58.
    Lee SJ, Liang L, Juarez S, Nanton MR, Gondwe EN, Msefula CL, Kayala MA, Necchi F, Heath JN, Hart P, Tsolis RM, Heyderman RS, MacLennan CA, Felgner PL, Davies DH, McSorley SJ (2012) Identification of a common immune signature in murine and human systemic Salmonellosis. Proc Natl Acad Sci U S A 109(13):4998–5003.  https://doi.org/10.1073/pnas.1111413109 Google Scholar
  59. 59.
    Wickham ME, Brown NF, Provias J, Finlay BB, Coombes BK (2007) Oral infection of mice with Salmonella enterica serovar Typhimurium causes meningitis and infection of the brain. BMC Infect Dis 7:65.  https://doi.org/10.1186/1471-2334-7-65 Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.School of Biological SciencesNational Institute of Science Education and Research (NISER), HBNIKhurdhaIndia
  2. 2.S. K. Dash Center of Excellence of Biosciences and Engineering & Technology (SKBET)Indian Institute of Technology BhubaneswarBhubaneswarIndia
  3. 3.Biozentrum der Universität BaselBaselSwitzerland
  4. 4.Bionivid Technology Private LimitedBengaluruIndia
  5. 5.Institute of Life SciencesBhubaneswarIndia

Personalised recommendations