Salmonella-induced changes of the rat intestinal microbiota

Cover Page


Cite item

Full Text

Abstract

The gut microbiome profoundly affects the body functioning: it participates in host protection against pathogenic microorganisms, metabolic events, inhibition of inflammatory responses, formation of innate and adaptive immune response in the intestinal mucosa. One of the causes altering microbiota community is due to antibiotics. Therefore, the processes of antibiotics interaction together with Salmonella enteritidis and Salmonella typhimurium with representatives of normal intestinal microflora are of particular interest. Materials and methods. The quantitative and qualitative analysis of the wall microbiota composition in rats was evaluated by bacteriological method, the statistical data analysis was performed using the software StatSoft Statistica v.12. Results and discussion. Inoculation of vancomycin and S. enteritidis, S. typhimurium in groups II, III, IV resulted in quantitatively decreased E. coli level by 10-, 7- and 110-fold, respectively (p ≤ 0.05). The count of P. aeruginosa decreased markedly only in the group III (p ≤ 0.05). The count of Bacteroides spp. members was profoundly decreased by several thousand times (group II) as well as 70- and 87-fold (groups III and IV), respectively (p ≤ 0.05). The count of E. faecalis and E. faecium decreased by 861-, 6- and several thousand times (groups II, III, IV), respectively (p ≤ 0.05). The count of Proteus spp. markedly decreased in group II by 27-fold and rapidly increased in group IV (p ≤ 0.05). Group III revealed a sharp decline in level of Enterobacter spp. and Klebsiella spp. by 847- and 150-fold, whereas in group II they were increased by 7- and 46-fold, respectively (p ≤ 0.05). The count of Staphylococcus spp. decreased by 10-fold only in group II. The level of Clostridium spp. decreased by several thousand times (group II) and by 5,500 times (group IV) (p ≤ 0.05). The count of Lactobacillus spp. decreased by several thousand times (group II). The count of Bifidobacterium spp. members significantly decreased by 10.9-fold and by several thousand times (groups III, IV). The level of Peptostreptococcus anaerobius profoundly decreased in all three study groups (p ≤ 0.05). The level of Salmonella spp. increased in group II by 49 times, but markedly increased in groups III and IV (p ≤ 0.05). Inoculation of Salmonella after vancomycin pretreatment caused dramatic change in the microbiota composition in groups V and VI, namely: increased count of E. coli by 65- and 105-fold, markedly increased level of P. aeruginosa in group V and VI — by 3-fold. In addition, these groups also showed decreased level of Bacteroides spp. by 9- and 10-fold (p ≤ 0.05). The count of E. faecalis and E. faecium decreased dramatically only in group V (p ≤ 0.05). The count of Proteus spp. decreased by 17 times in group V as well as in group VI (p ≤ 0.05). A sharp increase in level of Enterobacter spp. and Klebsiella spp. members was observed in groups V and VI (p ≤ 0.05). However, representatives of Peptostreptococcus anaerobius in groups V and VI decreased by 20 and 9 times, respectively (p ≤ 0.05). The count of Salmonella spp. decreased only in group V by 7 times (p ≤ 0,05). Inoculating experimental animals with B. fragilis conditioned with S. enteritidis, S. typhimurium and pretreated with vancomycin resulted in markedly decreased level of E. coli in group VII and VIII by 538 times (p ≤ 0.05). The count of P. aeruginosa in groups VII and VIII decreased profoundly, whereas level of Bacteroides spp. members was reciprocally increased (p ≤ 0.05). The level of Lactobacillus spp. decreased by 10.3 times only in group VI. The count of E. faecalis and E. faecium increased by 10 and 19 times in groups VII and VIII, respectively, whereas level of Proteus spp. decreased only in group VII by 322 times (p ≤ 0.05). In addition, a sharp decrease in level of Enterobacter spp. and Klebsiella spp. members (p ≤ 0.05) was found in groups VII and VIII. The count of Peptostreptococcus anaerobius and Lactobacillus spp. members was markedly increased by 7-, 12-, several thousand-fold and 40 times (groups VII and VIII, respectively) (p ≤ 0.05). The count of S. enteritidis and S. typhimurium in groups VII and VIII decreased rapidly (p ≤ 0.05). Conclusion. Inoculation of B. fragilis can be used in treatment of inflammatory bowel diseases or disorders with impaired gut barrier function.

About the authors

Yu. V. Bukina

Zaporozhye State Medical University

Author for correspondence.
Email: lingvus25@gmail.com
ORCID iD: 0000-0001-9529-3798

Yuliia V. Bukina,  Assistant, Microbiology, Virology and Immunology Department 

69035, Zaporozhye, Maiakovskiy pr., 26

Phone: +3 (8096) 400-46-26, +3 (8095) 512-09-29 

Ukraine

N. N. Polishchuk

Zaporizhzhia State Medical University

Email: natalyapolishchuck23@gmail.com
ORCID iD: 0000-0001-9529-3798

PhD (Medicine), Associate Professor, Department of Microbiology, Virology and Immunology 

Zaporozhye

Ukraine

H. V. Bachurin

Zaporizhzhia State Medical University

Email: bachuringv@ukr.net
ORCID iD: 0000-0001-9529-3798

PhD, MD (Medicine), Associate Professor, Department of Urology 

Zaporozhye

Ukraine

O. S. Cherkovska

Zaporizhzhia State Medical University

Email: cherkovska2007@ukr.net
ORCID iD: 0000-0002-9875-6409

PhD (Medicine), Associate Professor, Faculty Surgery Department 

Zaporozhye

Ukraine

O. L. Zinych

Zaporizhzhia State Medical University

Email: zinka130579@gmail.com
ORCID iD: 0000-0001-9529-3798

PhD (Medicine), Associate Professor, Department of Human Anatomy, Operative Surgery and Topographic Anatomy 

Zaporozhye

Ukraine

O. L. Lazaryk

Zaporizhzhia State Medical University

Email: alexandralazaryk@gmail.com
ORCID iD: 0000-0003-1937-1226

PhD (Medicine), Associate Professor, Department of Human Anatomy, Operative Surgery and Topographic Anatomy 

Zaporozhye

Ukraine

M. B. Bezugly

Zaporozhye State Medical University

Email: mbezugly@ukr.net
ORCID iD: 0000-0001-6515-9440

PhD (Medicine), Associate Professor, Ophthalmology Department 

Zaporozhye

Ukraine

References

  1. Букина Ю.В., Камышный А.М., Полищук Н.Н., Топол И.А. Сальмонелла-индуцированные изменения кишечной микробиоты и транскриптома генов иммунного ответа на фоне введения ванкомицина и Bacteroides fragilis // Патологiя. 2017. Т. 14, № 1 (39). С. 12–19. [Bukina Y.V., Kamyshnyi A.M., Polishchuk N.N., Topol I.A. Salmonella-induced changes in the gut microbiota and immune response genes transcriptome during administration of vancomycin and Bacteroides fragilis. Patologiya = Pathology, 2017, vol. 14, no. 1 (39), pp. 12–19. (In Russ.)] doi: 10.14739/2310-1237.2017.1.97504
  2. Awoniyi M., Miller S.I., Wilson C.B., Hajjar A.M., Smith K.D. Homeostatic regulation of Salmonella-induced mucosal inflammation and injury by IL-23. PLoS One, 2012, vol. 7, no. 5: e37311. doi: 10. 1371/journal.pone.0037311
  3. Barthel M., Hapfelmeier S., Quintanilla-Martinez L. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun., 2003, vol. 71, pp. 2839–2858. doi: 10. 1128/iai.71.5.2839-2858.2003
  4. Cani P.D., Possemiers S., Van de Wiele T., Guiot Y., Everard A., Rottier O. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut, 2009, vol. 58, pp. 1091–1093. doi: 10.1136/gut.2008.165886
  5. Cho I., Yamanishi S., Cox L., Methé B.A., Zavadil J., Li K. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature, 2012, vol. 488, pp. 621–626. doi: 10.1038/nature11400
  6. Corrêa-Oliveira R., Fachi J.L., Vieira A., Sato F.T., Vinolo M.A. Regulation of immune cell function by short-chain fatty acids. Clin. Transl. Immunol., 2016, vol. 22, no. 5 (4): e73. doi: 10.1038/cti.2016.17
  7. Deplancke B., Gaskins Deplancke H.R. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am. J. Clin. Nutr., 2001, vol. 73, pp. 1131–1141. doi: 10.1093/ajcn/73.6.1131S
  8. El Aidy S., van Baarlen P., Derrien M., Lindenbergh-Kortleve D.J., Hooiveld G., Levenez F. Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. Mucosal Immunol., 2012, pp. 5567–5579. doi: 10.1038/mi.2012.32
  9. Ferreira R.B., Gill N., Willing B.P., Antunes L.C., Russell S.L., Croxen M.A., Finlay B.B. The intestinal microbiota plays a role in Salmonella-induced colitis independent of pathogen colonization. PLoS One, 2011, no. 6 (5): e20338. doi: 10.1371/journal.pone.0020338
  10. Grassl G., Finlay B. Pathogenesis of enteric Salmonella infections. Curr. Opin. Gastroenterol., 2008, vol. 24, pp. 22–26. doi: 10.1097/MOG.0b013e3282f21388
  11. Identification of Procaryotes. In: Bergey’s manual of systematic bacteriology. Volume 3: The Firmicutes. Ed. by Vos P., Garrity G., Jones D., Krieg N.R., Ludwig W., Rainey F.A., Schleifer K.-H., Whitman W. New York: Springer-Verlag New York, 2009. P. 1422.
  12. Jernberg C., Löfmark S., Edlund C., Jansson J.K. Long-term impacts of antibiotic exposure on the human intestinal microbiota. ISME J., 2007, vol. 1, pp. 56–66. doi: 10.1038/ismej.2007.3.
  13. Kau A.L., Ahern P.P., Griffin N.W., Goodman A.L., Gordon J.I. Human nutrition, the gut microbiome and the immune system. Nature, 2011, vol. 474, no. 7351, pp. 327–336. doi: 10.1038/nature10213
  14. Kerckhoffs A.P., Samson M., van der Rest M.E. Lower Bifidobacteria counts in both duodenal mucosa-associated and fecal microbiota in irritable bowel syndrome patients. World J. Gastroenterol., 2009, vol. 15, no. 23, pp. 2887–2892. doi: 10.3748/wjg.15.2887
  15. Lleal M., Sarrabayrouse G., Willamil J., Santiago A., Pozuelo M., Manichanh C. A single faecal microbiota transplantation modulates the microbiome and improves clinical manifestations in a rat model of colitis. EBioMedicine, 2019, vol. 48, pp. 630–641. doi: 10.1016/j.ebiom.2019.10.002
  16. Macpherson N.L., Harris Macpherson A.J. Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol., 2004, vol. 4, no. 6, pp. 478–485. doi: 10.1038/nri1373
  17. Maslowski K.M., Vieira A.T., Ng A., Kranich J., Sierro F., Yu D., Schilter H.C., Rolph M.S., Mackay F., Artis D., Xavier R.J., Teixeira M.M., Mackay C.R. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature, 2009, vol. 29, no. 7268, pp. 1282–1286. doi: 10.1038/nature08530
  18. Miki T., Goto R., Fujimoto M., Okada N., Hardt W.D. The bactericidal lectin RegIIIβ prolongs gut colonization and enteropathy in the streptomycin mouse model for salmonella diarrhea. Cell Host. Microbe, 2017, vol. 21, no. 2, pp. 195–207. doi: 10.1016/j.chom.2016.12.008
  19. Monack D.M., Bouley D.M., Falkow S.J. Salmonella typhimurium persists with in macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/+ mice and can be reactivated by IFNgamma neutralization. J. Exp. Med., 2004, vol. 199, no. 2, pp. 231–241. doi: 10.1084/jem.20031319
  20. Mu H., Bai H., Sun F., Liu Y., Lu Ch., Qiu Y., Chen P., Yang Y., Kong L., Duan J. Pathogen-targeting glycovesicles as a therapy for salmonellosis. Nat. Commun., 2019, vol. 10: 4039. doi: 10.1038/s41467-019-12066-z
  21. Nagpal R., Wang S., Solberg Woods L.C. Comparative microbiome signatures and short-chain fatty acids in mouse, rat, nonhuman primate, and human feces. Front Microbiol., 2018, vol. 9: 2897. doi: 10.3389/fmicb.2018.02897
  22. Panda S., Elkhader I., Casellas F., López Vivancos J., García Cors M., Santiago A., Cuenca S., Guarner F., Manichanh C. Shortterm effect of antibiotics on human gut microbiota. PLoS One, 2014, vol. 9, no. 4: e95476. doi: 10.1371/journal.pone.0095476
  23. Parkes G.C., Rayment N.B., Hudspith B.N. Distinct microbial population exist in the mucosal-associated microbiota of subgroups of irritable bowel syndrome. Neurogastroenterol Motil., 2012, vol. 24, no. 1, pp. 31–39. doi: 10. 10.1111/j.1365-2982.2011.01803.x
  24. Pérez-Cobas A.E., Artacho A., Knecht H., Ferrús M.L., Friedrichs A., Ott S.J. Differential effects of antibiotic therapy on the structure and function of human gut microbiota. PLoS One, 2013, vol. 8, no. 11: e80201. doi: 10.1371/journal.pone.0080201
  25. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F. Recognition of commensally microflora by toll-like receptors is required for intestinal homeostasis. Cell, 2004, vol. 118, no. 2, pp. 229–241. doi: 10.1016/j.cell.2004.07.002
  26. Santos R.L., Raffatellu M., Bevins C.L., Adams L.G., Tukel C., Tsolis R.M., Baumler A.J. Life in the inflamed intestine, Salmonella style. PubMed, 2009, vol. 17, no. 11, pp. 498–506. doi: 10.1016/j.tim.2009.08.008
  27. Sekirov I., Tam N.M., Jogova M., Robertson M.L., Li Y. Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. PubMed, 2008, vol. 76, no. 10, pp. 4726–4736. doi: 10.1128/IAI.00319-08
  28. Song H.J., Shim K.N., Jung S.A., Choi H.J., Lee M.A., Ryu K.H., Kim S.E., Yoo K. Antibiotic-associated diarrhea. Korean J. Intern. Med., 2008, vol. 23, pp. 9–15. doi: 10.3904/kjim.2008.23.1.9
  29. Stecher B., Chaffron S., Käppeli R., Hapfelmeier S., Freedrich S., Weber T.C., Kirundi J., Suar M., McCoy K.D., von Mering C., Macpherson A.J., Hardt W.D. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog, 2010, vol. 6, no. 1: e1000711. doi: 10.1371/journal.ppat.1000711
  30. Stecher B., Hardt W.D. Mechanisms controlling pathogen colonization of the gut. Curr. Opin. Microbiol., 2011, vol. 14, no. 1, pp. 82–91. doi: 10.1016/j.mib.2010.10.003
  31. Stecher B., Hardt W.D. The role of microbiota in infectious disease. Trends Microbiol., 2008, vol. 16, no. 3, pp. 107–114. doi: 10.1016/j.tim.2007.12.008
  32. Surana N.K., Kasper D.L. The yin yang of bacterial polysaccharides: lessons learned from B. fragilis PSA. Immunol. Rev., 2012, vol. 245, no. 1, pp. 13–26. doi: 10.1111/j.1600-065X.2011.01075.x
  33. Taylor D.N., McKenzie R., Durbin A., Carpenter C., Atzinger C.B., Haake R., Bourgeois A.L. Rifaximin, a nonabsorbed oral antibiotic, prevents shigellosis after experimental challenge. Clin. Infect. Dis., 2006, vol. 42, no. 9, pp. 1283–1288. doi: 10.1086/503039
  34. Turnbaugh P.J., Ley R.E., Mahowald M.A., Magrini V., Mardis E.R. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 2006, vol. 444, no. 7122, pp. 1027–1031. doi: 10.1038/nature05414
  35. Ubeda C., Pamer E.G. Antibiotics, microbiota and immune defense. Trends Immunol., 2012, vol. 33, no. 9, pp. 459–466. doi: 10.1016/j.it.2012.05.003
  36. Ubeda C., Taur Y., Jenq R.R., Equinda M.J., Son T., Samstein M., Viale A., Socci N.D., van den Brink M.R., Kamboj M., Pamer E.G. Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J. Clin. Invest., 2010, vol. 120, no. 12, pp. 4332–4341. doi: 10.1172/JCI43918
  37. Vollaard E.J., Clasener H.A. Colonization resistance. Antimicrob. Agents Chemother., 1994, vol. 38, no. 3, pp. 409–414. doi: 10. 10.1128/aac.38.3.409
  38. Wlodarska M., Willing B., Keeney K.M., Menendez A., Bergstrom K.S., Gill N. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun., 2011, vol. 79, no. 4, pp. 1536– 1545. doi: 10.1128/IAI.01104-10
  39. Zeng H., Chi H. Metabolic control of regulatory T cell development and function. Trends Immunol., 2015, vol. 36, no. 1, pp. 3–12. doi: 10.1016/j.it.2014.08.003
  40. Zhang Y., Limaye P.B., Renaud H.J., Klaassen C.D. Effect of various antibiotics on modulation of intestinal microbiota and bile acid profile in mice. Toxicol. Appl. Pharmacol., 2014, vol. 277, no. 2, pp. 138–145. doi: 10.1016/j.taap.2014.03.009
  41. Сarroll I.M., Chang Y.H., Park J. Luminal and mucosal-associated intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Gut Pathogenes., 2010, vol. 2: 19. doi: 10.1186/1757-4749-2-19

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2021 Bukina Y.V., Polishchuk N.N., Bachurin H.V., Cherkovska O.S., Zinych O.L., Lazaryk O.L., Bezugly M.B.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies