Skip to main content
Log in

Probiotics and Probiotic Metabolic Product Improved Intestinal Function and Ameliorated LPS-Induced Injury in Rats

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

In the present study, we sought to determine the effects of Bacillus subtilis (BAS) and Bacillus licheniformis (BAL) in rats after lipopolysaccharide (LPS)-induced acute intestinal inflammation. We also determined whether the B. subtilis metabolic product (BASM) is as effective as the live-cell probiotic. 60 male SD rats were randomly assigned to five groups and administered a diet containing 0.05% B. licheniformis (BAL group), 0.05% B. subtilis (BAS group), 0.5% B. subtilis metabolic product (BASM group), or a basic diet (PC group and NC group) for 40 days. On day 40, BAL, BAS, BASM, and NC groups were injected with 4 mg/kg body weight LPS. 4 h later, all rats were anesthetized and sacrificed. The results showed that the administration of B. licheniformis and B. subtilis improved intestinal function as evidenced by histology, increased enzyme activity, and mucosal thickness. They also increased the number of intraepithelial lymphocytes and decreased mucosal myeloperoxidase activity and plasma TNF-α. In addition, the cecal content of B. subtilis-treated rats had significantly increased microbial diversity, decreased numbers of Firmicutes, and increased numbers of Bacteroidetes as compared to rats fed basic diets. Similar to BAS group, the cecal content of B. licheniformis-treated rats decreased the number of Firmicutes. Administration of B. subtilis metabolic product had similar effects on intestinal function, inflammation response, and microbial diversity as B. subtilis but these effects were attenuated. In conclusion, administration of probiotic strains B. licheniformis or B. subtilis improved intestinal function, ameliorated the inflammation response, and modulated microflora after LPS-induced acute inflammation in rats. Non-living cells also exerted probiotic properties but live cells tended to function better.

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

Access this article

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
Fig. 9

Similar content being viewed by others

References

  1. Arribas B, Rodríguezcabezas ME, Camuesco D, Comalada M, Bailón E, Utrilla P, Nieto A, Concha A, Zarzuelo A, Gálvez J (2009) A probiotic strain of Escherichia coli, Nissle 1917, given orally exerts local and systemic anti-inflammatory effects in lipopolysaccharide-induced sepsis in mice. Br J Pharmacol 157:1024–1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Asai KI, Komine Y, Kozutsumi T, Yamaguchi T, Komine KI, Kumagai K (2000) Predominant subpopulations of t lymphocytes in the mammary gland secretions during lactation and intraepithelial T lymphocytes in the intestine of dairy cows. Vet Immunol Immunopathol 73:233–240

    Article  CAS  PubMed  Google Scholar 

  3. Bordoni A, Amaretti A, Leonardi A, Boschetti E, Danesi F, Matteuzzi D, Roncaglia L, Raimondi S, Rossi M (2013) Cholesterol-lowering probiotics: in vitro selection and in vivo testing of Bifidobacteria. Appl Microbiol Biotechnol 97:8273–8281

    Article  CAS  PubMed  Google Scholar 

  4. Choi JY, Kim JS, Ingale SL, Kim KH, Shinde PL, Kwon IK et al (2011) Effect of potential multimicrobe probiotic product processed by high drying temperature and antibiotic on performance of weanling pigs. J Anim Sci 89:1795–1804

    Article  CAS  PubMed  Google Scholar 

  5. Collington GK, Parker DS, Armstrong DG (1990) The influence of inclusion of either an antibiotic or a probiotic in the diet on the development of digestive enzyme activity in the pig. Br J Nutr 64:59–70

    Article  CAS  PubMed  Google Scholar 

  6. Deng W, Dong XF, Tong JM, Zhang Q (2012) The probiotic Bacillus licheniformis ameliorates heat stress-induced impairment of egg production, gut morphology, and intestinal mucosal immunity in laying hens. Poult Sci 91:575–582

    Article  CAS  PubMed  Google Scholar 

  7. Eutamene H, Lamine F, Chabo C, Theodorou V, Rochat F, Bergonzelli GE, Corthésy-Theulaz I, Fioramonti J, Bueno L (2007) Synergy between Lactobacillus paracasei and its bacterial products to counteract stress-induced gut permeability and sensitivity increase in rats. J Nutr 137:1901–1907

    CAS  PubMed  Google Scholar 

  8. Fernández MF, Boris S, Barbés C (2003) Probiotic properties of human lactobacilli strains to be used in the gastrointestinal tract. J Appl Microbiol 94:449–455

    Article  PubMed  Google Scholar 

  9. Gareau MG, Sherman PM, Walker WA (2010) Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 7:503–514

    Article  PubMed  PubMed Central  Google Scholar 

  10. Giang HH, Viet TQ, Ogle B, Lindberg JE (2010) Growth performance, digestibility, gut environment and health status in weaned piglets fed a diet supplemented with potentially probiotic complexes of lactic acid bacteria. Livest Sci 129:95–103

    Article  Google Scholar 

  11. Goyal N, Rishi P, Shukla G (2013) Lactobacillus rhamnosus, GG antagonizes giardia intestinalis, induced oxidative stress and intestinal disaccharidases: an experimental study. World J Microbiol Biotechnol 29:1049–1057

    Article  PubMed  Google Scholar 

  12. Guo Z, Liu XM, Zhang QX, Shen Z, Tian FW, Zhang H, Sun ZH, Zhang HP, Chen W (2011) Influence of consumption of probiotics on the plasma lipid profile: a meta-analysis of randomised controlled trials. Nutr Metab Cardiovasc Dis 21:844–850

    Article  CAS  PubMed  Google Scholar 

  13. Hardy H, Harris J, Lyon E, Beal J, Foey AD (2013) Probiotics, prebiotics and immunomodulation of gut mucosal defences: homeostasis and immunopathology. Nutrients 5:1869–1912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Henker J, Laass MW, Blokhin BM, Maydannik VG, Bolbot YK, Elze M, Wolff C, Schreiner A, Schulze J (2008) Probiotic Escherichia coli Nissle 1917 versus placebo for treating diarrhea of greater than 4 days duration in infants and toddlers. Pediatr Infect Dis J 27:494–499

    Article  PubMed  Google Scholar 

  15. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, 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

    Article  PubMed  Google Scholar 

  16. Hoarau C, Lagaraine C, Martin L, Velge-Roussel F, Lebranchu Y (2006) Supernatant of Bifidobacterium breve induces dendritic cell maturation, activation, and survival through a Toll-like receptor 2 pathway. J Allergy Clin Immunol 117:696–702

    Article  CAS  PubMed  Google Scholar 

  17. Kaakoush NO (2015) Insights into the role of Erysipelotrichaceae in the human host. Front Cell Infect Microbiol 5:84

    Article  PubMed  PubMed Central  Google Scholar 

  18. Kang JH, Yun SI, Park MH, Park JH, Jeong SY, Park HO (2013) Anti-obesity effect of Lactobacillus gasseri bnr17 in high-sucrose diet-induced obese mice. PLoS ONE 8:e54617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kerckhoffs AP, Samsom M, van der Rest ME, de Vogel J, Knol J, Ben-Amor K, Akkermans LM (2009) Lower Bifidobacteria counts in both duodenal mucosa-associated and fecal microbiota in irritable bowel syndrome patients. World J Gastroenterol 15:2887–2892

    Article  PubMed  PubMed Central  Google Scholar 

  20. Lee JH, Lee B, Lee HS, Bae EA, Lee H, Ahn YT, Lim KS, Huh CS, Kim DH (2009) Lactobacillus suntoryeus inhibits pro-inflammatory cytokine expression and tlr-4-linked nf-kappab activation in experimental colitis. Int J Colorectal Dis 24:231–237

    Article  PubMed  Google Scholar 

  21. Lee YK (2013) Effects of diet on gut microbiota profile and the implications for health and disease. Biosci Microb Food Health 32:1–12

    Article  Google Scholar 

  22. Leser TD, Knarreborg A, Worm J (2008) Germination and outgrowth of Bacillus subtilis and Bacillus licheniformis spores in the gastrointestinal tract of pigs. J Appl Microbiol 104:1025–1033

    Article  CAS  PubMed  Google Scholar 

  23. Lesniewska V, Rowland I, Cani PD, Neyrinck AM, Delzenne NM, Naughton PJ (2006) Effect on components of the intestinal microflora and plasma neuropeptide levels of feeding Lactobacillus delbrueckii, Bifidobacterium lactis, and inulin to adult and elderly rats. Appl Environ Microbiol 72:6533–6538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023

    Article  CAS  PubMed  Google Scholar 

  25. Li X, Qiang L, Xu C (2008) Effects of supplementation of fructooligosaccharide and/or Bacillus subtilis to diets on performance and on intestinal microflora in broilers. Arch Tierz 51:64–70

    CAS  Google Scholar 

  26. Meresse D, Harmand S, Siroux M, Watremez M, Dubar L (2012) Probiotics stimulate enterocyte migration and microbial diversity in the neonatal mouse intestine. FASEB J 26:1960–1969

    Article  Google Scholar 

  27. Moore T, Globa L, Pustovyy O, Vodyanoy V, Sorokulova I (2014) Oral administration of Bacillus subtilis, strain bsb3 can prevent heat stress-related adverse effects in rats. J Appl Microbiol 117:1463–1471

    Article  CAS  PubMed  Google Scholar 

  28. Naito E, Yoshida Y, Makino K, Kounoshi Y, Kunihiro S, Takahashi R, Matsuzaki T, Miyazaki K, Ishikawa F (2011) Beneficial effect of oral administration of Lactobacillus casei strain Shirota on insulin resistance in diet-induced obesity mice. J Appl Microbiol 110:650–657

    Article  CAS  PubMed  Google Scholar 

  29. Otte JM, Podolsky DK (2004) Functional modulation of enterocytes by gram-positive and gram-negative microorganisms. Am J Physiol Gastrointest Liver Physiol 286:613–626

    Article  Google Scholar 

  30. Pagnini C, Saeed R, Bamias G, Arseneau KO, Pizarro TT, Cominelli F (2010) Probiotics promote gut health through stimulation of epithelial innate immunity. Proc Natl Acad Sci USA 107:454–459

    Article  CAS  PubMed  Google Scholar 

  31. Paterson DL (2006) Resistance in gram-negative bacteria: Enterobacteriaceae. Am J Med 119:62–70

    Article  Google Scholar 

  32. Perić LI, Milošević NI, Žikić D, Bjedov SI, Cvetković D, Markov SI, Mohnl MI, Steiner TO (2010) Effects of probiotic and phytogenic products on performance, gut morphology and cecal microflora of broiler chickens. Arch Tierz 53:350–359

    Google Scholar 

  33. Purwandari A, Chen HY (2013) Effects of probiotic Bacillus subtilis on intestinal microbial diversity and immunity of orange spotted grouper Epinephelus coioides. J Appl Biotechnol 1:25–36

    Article  Google Scholar 

  34. Rajilić-Stojanović M, Shanahan F, Guarner F, de Vos WM (2013) Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Inflamm Bowel Dis 19:481–488

    Article  PubMed  Google Scholar 

  35. Resta-Lenert S, Barrett KE (2006) Probiotics and commensals reverse TNF-alpha and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 130:731–746

    Article  CAS  PubMed  Google Scholar 

  36. Resta-Lenert S, Barrett KE (2003) Live probiotics protect intestinal epithelial cells from the effects of infection with enteroinvasive Escherichia coli (EIEC). Gut 52:988–997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Rieger J, Janczyk P, Hünigen H, Neumann K, Plendl J (2015) Intraepithelial lymphocyte numbers and histomorphological parameters in the porcine gut after enterococcus faecium, ncimb 10415 feeding in a salmonella, typhimurium challenge. Vet Immunol Immunopathol 164:40–50

    Article  CAS  PubMed  Google Scholar 

  38. Rinttilä T, Apajalahti J (2013) Intestinal microbiota and metabolites—implications for broiler chicken health and performance. J Appl Poult Res 22:647–658

    Article  Google Scholar 

  39. Ross GR, Gusils C, Oliszewski R, de Holgado SC, González SN (2010) Effects of probiotic administration in swine. J Biosci Bioeng 109:545–549

    Article  CAS  PubMed  Google Scholar 

  40. Shanahan F (2004) Host-flora interactions in inflammatory bowel disease. Inflamm Bowel Dis 10:16–24

    Article  Google Scholar 

  41. Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper K, van Capel TM, Zaat BA, Yazdanbakhsh M, Wierenga EA, van Kooyk Y, Kapsenberg ML (2005) Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J Allergy Clin Immunol 115:1260–1267

    Article  CAS  PubMed  Google Scholar 

  42. Tannock GW, Munro K, Harmsen HJ, Welling GW, Smart J, Gopal PK (2000) Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Appl Environ Microbiol 66:2578–2588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI (2009) A core gut microbiome in obese and lean twins. Nature 457:480–484

    Article  CAS  PubMed  Google Scholar 

  44. Turroni F, Serafini F, Foroni E, Duranti S, O’Connell Motherway M, Taverniti V, Mangifesta M, Milani C, Viappiani A, Roversi T, Sánchez B, Santoni A, Gioiosa L, Ferrarini A, Delledonne M, Margolles A, Piazza L, Palanza P, Bolchi A, Guglielmetti S, van Sinderen D, Ventura M (2013) Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium–host interactions. Proc Natl Acad Sci USA 110:11151–11156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Velagapudi VR, Hezaveh R, Reigstad CS, Gopalacharyulu P, Yetukuri L, Islam S, Felin J, Perkins R, Borén J, Oresic M, Bäckhed F (2010) The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res 51:1101–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Wang J, Huang T, Zhang C, Zhao Y, Derrien M, Rocher E, van Hylckama Vlieg JE, Strissel K, Zhao L, Obin M, Shen J (2015) Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J 9:1–15

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by grants from the Special Fund for Agro-scientific Research in the Public Interest (No. 201403047). The authors report no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ziwei Xu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deng, B., Wu, J., Li, X. et al. Probiotics and Probiotic Metabolic Product Improved Intestinal Function and Ameliorated LPS-Induced Injury in Rats. Curr Microbiol 74, 1306–1315 (2017). https://doi.org/10.1007/s00284-017-1318-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-017-1318-7

Navigation