Cattle intestinal microbiota shifts following Escherichia coli O157:H7 vaccination and colonizationtravel


Autoři: Raies A. Mir aff001;  Robert G. Schaut aff001;  Heather K. Allen aff001;  Torey Looft aff001;  Crystal L. Loving aff001;  Indira T. Kudva aff001;  Vijay K. Sharma aff001
Působiště autorů: Food Safety and Enteric Pathogens Research Unit, National Animal Disease Center, Agricultural Research Service, U.S. Department of Agriculture, Ames, IA, United States of America aff001;  Oak Ridge Institute for Science and Education (ORISE), ARS Research Participation Program, Oak Ridge, TN, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226099

Souhrn

Vaccination-induced Escherichia coli O157:H7-specific immune responses have been shown to reduce E. coli O157:H7 shedding in cattle. Although E. coli O157:H7 colonization is correlated with perturbations in intestinal microbial diversity, it is not yet known whether vaccination against E. coli O157:H7 could cause shifts in bovine intestinal microbiota. To understand the impact of E. coli O157:H7 vaccination and colonization on intestinal microbial diversity, cattle were vaccinated with two doses of different E. coli O157:H7 vaccine formulations. Six weeks post-vaccination, the two vaccinated groups (Vx-Ch) and one non-vaccinated group (NonVx-Ch) were orally challenged with E. coli O157:H7. Another group was neither vaccinated nor challenged (NonVx-NonCh). Fecal microbiota analysis over a 30-day period indicated a significant (FDR corrected, p <0.05) association of bacterial community structure with vaccination until E. coli O157:H7 challenge. Shannon diversity index and species richness were significantly lower in vaccinated compared to non-vaccinated groups after E. coli O157:H7 challenge (p < 0.05). The Firmicutes:Bacteroidetes ratio (p > 0.05) was not associated with vaccination but the relative abundance of Proteobacteria was significantly lower (p < 0.05) in vaccinated calves after E. coli O157:H7 challenge. Similarly, Vx-Ch calves had higher relative abundance of Paeniclostridium spp. and Christenellaceae R7 group while Campylobacter spp., and Sutterella spp. were more abundant in NonVx-Ch group post-E. coli O157:H7 challenge. Only Vx-Ch calves had significantly higher (p < 0.001) E. coli O157:H7-specific serum IgG but no detectable E. coli O157:H7-specific IgA. However, E. coli O157:H7-specific IL-10-producing T cells were detected in vaccinated animals prior to challenge, but IFN-γ-producing T cells were not detected. Neither E. coli O157:H7-specific IgG nor IgA were detected in blood or feces, respectively, of NonVx-Ch and NonVx-NonCh groups prior to or post vaccinations. Both Vx-Ch and NonVx-Ch animals shed detectable levels of challenge strain during the course of the study. Despite the lack of protection with the vaccine formulations there were detectable shifts in the microbiota of vaccinated animals before and after challenge with E. coli O157:H7.

Klíčová slova:

Bacteria – Cattle – Community structure – Immune response – Microbiome – Molting – Vaccination and immunization – Vaccines


Zdroje

1. Davis MA, Cloud-Hansen KA, Carpenter J, Hovde CJ. Escherichia coli O157:H7 in environments of culture-positive cattle. Appl Environ Microbiol. 2005;71(11):6816–22. Epub 2005/11/05. doi: 10.1128/AEM.71.11.6816-6822.2005 16269714; PubMed Central PMCID: PMC1287631.

2. Naylor SW, Low JC, Besser TE, Mahajan A, Gunn GJ, Pearce MC, et al. Lymphoid Follicle-Dense Mucosa at the Terminal Rectum Is the Principal Site of Colonization of Enterohemorrhagic Escherichia coli O157:H7 in the Bovine Host. Infection and Immunity. 2003;71(3):1505–12. doi: 10.1128/IAI.71.3.1505-1512.2003 12595469

3. Pruimboom-Brees IM, Morgan TW, Ackermann MR, Nystrom ED, Samuel JE, Cornick NA, et al. Cattle lack vascular receptors for Escherichia coli O157:H7 Shiga toxins. Proc Natl Acad Sci U S A. 2000;97(19):10325–9. Epub 2000/09/06. doi: 10.1073/pnas.190329997 10973498; PubMed Central PMCID: PMC27023.

4. Davis TK, Van De Kar NC, Tarr PI. Shiga Toxin/Verocytotoxin-Producing Escherichia coli Infections: Practical Clinical Perspectives. Microbiol Spectr. 2014;2(4):EHEC-0025-2014. Epub 2015/06/25. doi: 10.1128/microbiolspec.EHEC-0025-2014 26104210.

5. Riley LW, Remis RS, Helgerson SD, McGee HB, Wells JG, Davis BR, et al. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med. 1983;308(12):681–5. Epub 1983/03/24. doi: 10.1056/NEJM198303243081203 6338386.

6. Elder RO, Keen JE, Siragusa GR, Barkocy-Gallagher GA, Koohmaraie M, Laegreid WW. Correlation of enterohemorrhagic Escherichia coli O157 prevalence in feces, hides, and carcasses of beef cattle during processing. Proc Natl Acad Sci USA. 2000;97(7):5.

7. Matthews L, Reeve R, Gally DL, Low JC, Woolhouse ME, McAteer SP, et al. Predicting the public health benefit of vaccinating cattle against Escherichia coli O157. Proc Natl Acad Sci U S A. 2013;110(40):16265–70. Epub 2013/09/18. doi: 10.1073/pnas.1304978110 24043803; PubMed Central PMCID: PMC3791763.

8. Varela NP, Dick P, Wilson J. Assessing the Existing Information on the Efficacy of Bovine Vaccination against Escherichia coli O157:H7 A Systematic Review and Meta-analysis. Zoonoses Public Hlth. 2013;60(4):253–68. doi: 10.1111/j.1863-2378.2012.01523.x WOS:000318098500001. 22856462

9. Fox JT, Thomson DU, Drouillard JS, Thornton AB, Burkhardt DT, Emery DA, et al. Efficacy of Escherichia coli O157:H7 siderophore receptor/porin proteins-based vaccine in feedlot cattle naturally shedding E. coli O157. Foodborne Pathog Dis. 2009;6(7):893–9. Epub 2009/09/10. doi: 10.1089/fpd.2009.0336 19737065.

10. Potter AA, Klashinsky S, Li Y, Frey E, Townsend H, Rogan D, et al. Decreased shedding of Escherichia coli O157:H7 by cattle following vaccination with type III secreted proteins. Vaccine. 2004;22(3–4):362–9. Epub 2003/12/13. doi: 10.1016/j.vaccine.2003.08.007 14670317.

11. Stanford K, Hannon S, Booker CW, Jim GK. Variable efficacy of a vaccine and direct-fed microbial for controlling Escherichia coli O157:H7 in feces and on hides of feedlot cattle. Foodborne Pathog Dis. 2014;11(5):379–87. Epub 2014/03/29. doi: 10.1089/fpd.2013.1693 24673729.

12. Thomson DU, Loneragan GH, Thornton AB, Lechtenberg KF, Emery DA, Burkhardt DT, et al. Use of a siderophore receptor and porin proteins-based vaccine to control the burden of Escherichia coli O157:H7 in feedlot cattle. Foodborne Pathog Dis. 2009;6(7):871–7. Epub 2009/09/10. doi: 10.1089/fpd.2009.0290 19737063.

13. Sharma VK, Dean-Nystrom EA, Casey TA. Evaluation of hha and hha sepB mutant strains of Escherichia coli O157:H7 as bacterins for reducing E. coli O157:H7 shedding in cattle. Vaccine. 2011;29(31):5078–86. Epub 2011/05/10. doi: 10.1016/j.vaccine.2011.04.073 21550373.

14. Sharma VK, Schaut RG, Loving CL. Vaccination with killed whole-cells of Escherichia coli O157:H7 hha mutant emulsified with an adjuvant induced vaccine strain-specific serum antibodies and reduced E. coli O157:H7 fecal shedding in cattle. Vet Microbiol. 2018;219:190–9. Epub 2018/05/21. doi: 10.1016/j.vetmic.2018.04.003 29778196.

15. Nguyen QN, Himes JE, Martinez DR, Permar SR. The Impact of the Gut Microbiota on Humoral Immunity to Pathogens and Vaccination in Early Infancy. PLoS Pathog. 2016;12(12):e1005997. Epub 2016/12/23. doi: 10.1371/journal.ppat.1005997 28006021; PubMed Central PMCID: PMC5179050.

16. Oh JZ, Ravindran R, Chassaing B, Carvalho FA, Maddur MS, Bower M, et al. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity. 2014;41(3):478–92. Epub 2014/09/16. doi: 10.1016/j.immuni.2014.08.009 25220212; PubMed Central PMCID: PMC4169736.

17. Mao S, Zhang M, Liu J, Zhu W. Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle: membership and potential function. Sci Rep. 2015;5:16116. Epub 2015/11/04. doi: 10.1038/srep16116 26527325; PubMed Central PMCID: PMC4630781.

18. Callaway TR, Dowd SE, Edrington TS, Anderson RC, Krueger N, Bauer N, et al. Evaluation of bacterial diversity in the rumen and feces of cattle fed different levels of dried distillers grains plus solubles using bacterial tag-encoded FLX amplicon pyrosequencing. J Anim Sci. 2010;88(12):3977–83. Epub 2010/08/24. doi: 10.2527/jas.2010-2900 20729286.

19. Thomas M, Webb M, Ghimire S, Blair A, Olson K, Fenske GJ, et al. Metagenomic characterization of the effect of feed additives on the gut microbiome and antibiotic resistome of feedlot cattle. Sci Rep. 2017;7(1):12257. Epub 2017/09/28. doi: 10.1038/s41598-017-12481-6 28947833; PubMed Central PMCID: PMC5612972.

20. Myer PR, Freetly HC, Wells JE, Smith TPL, Kuehn LA. Analysis of the gut bacterial communities in beef cattle and their association with feed intake, growth, and efficiency. Journal of Animal Science. 2017;95(7). doi: 10.2527/jas2016.1059

21. Petri RM, Schwaiger T, Penner GB, Beauchemin KA, Forster RJ, McKinnon JJ, et al. Characterization of the core rumen microbiome in cattle during transition from forage to concentrate as well as during and after an acidotic challenge. PLoS One. 2013;8(12):e83424. Epub 2014/01/07. doi: 10.1371/journal.pone.0083424 24391765; PubMed Central PMCID: PMC3877040.

22. Benckert J, Schmolka N, Kreschel C, Zoller MJ, Sturm A, Wiedenmann B, et al. The majority of intestinal IgA+ and IgG+ plasmablasts in the human gut are antigen-specific. J Clin Invest. 2011;121(5):1946–55. Epub 2011/04/15. doi: 10.1172/JCI44447 21490392; PubMed Central PMCID: PMC3083800.

23. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, et al. Induction of Colonic Regulatory T Cells by Indigenous Clostridium Species. Science. 2011;331:5. doi: 10.1126/science.1198469 21205640

24. Jami E, White BA, Mizrahi I. Potential role of the bovine rumen microbiome in modulating milk composition and feed efficiency. PLoS One. 2014;9(1):e85423. Epub 2014/01/28. doi: 10.1371/journal.pone.0085423 24465556; PubMed Central PMCID: PMC3899005.

25. Li Q, Lauber CL, Czarnecki-Maulden G, Pan Y, Hannah SS. Effects of the Dietary Protein and Carbohydrate Ratio on Gut Microbiomes in Dogs of Different Body Conditions. MBio. 2017;8(1). Epub 2017/01/26. doi: 10.1128/mBio.01703-16 28119466; PubMed Central PMCID: PMC5263242.

26. Sampson TR, Debelius JW, Thron T, Janssen S, Shastri GG, Ilhan ZE, et al. Gut Microbiota Regulate Motor Deficits and Neuroinflammation in a Model of Parkinson's Disease. Cell. 2016;167(6):1469–80 e12. Epub 2016/12/03. doi: 10.1016/j.cell.2016.11.018 27912057; PubMed Central PMCID: PMC5718049.

27. Lima FS, Oikonomou G, Lima SF, Bicalho ML, Ganda EK, Filho JC, et al. Prepartum and postpartum rumen fluid microbiomes: characterization and correlation with production traits in dairy cows. Appl Environ Microbiol. 2015;81(4):1327–37. Epub 2014/12/17. doi: 10.1128/AEM.03138-14 25501481; PubMed Central PMCID: PMC4309715.

28. Sharma VK, Bayles DO, Alt DP, Looft T. Complete Genome Sequences of Curli-Negative and Curli-Positive Isolates of Foodborne Escherichia coli O157:H7 Strain 86–24. Genome Announc. 2016;4(6). Epub 2016/12/17. doi: 10.1128/genomeA.01323-16 27979932; PubMed Central PMCID: PMC5159565.

29. Sharma VK, Zuerner RL. Role of hha and ler in transcriptional regulation of the esp operon of enterohemorrhagic Escherichia coli O157:H7. J Bacteriol. 2004;186(21):7290–301. Epub 2004/10/19. doi: 10.1128/JB.186.21.7290-7301.2004 15489441; PubMed Central PMCID: PMC523200.

30. Schaut RG, Boggiatto PM, Loving CL, Sharma VK. Cellular and Mucosal Immune Responses Following Vaccination with Inactivated Mutant of Escherichia coli O157:H7. Sci Rep. 2019;9(1):6401. Epub 2019/04/27. doi: 10.1038/s41598-019-42861-z 31024031; PubMed Central PMCID: PMC6483982.

31. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79(17):5112–20. Epub 2013/06/25. doi: 10.1128/AEM.01043-13 23793624; PubMed Central PMCID: PMC3753973.

32. Allen HK, Bayles DO, Looft T, Trachsel J, Bass BE, Alt DP, et al. Pipeline for amplifying and analyzing amplicons of the V1-V3 region of the 16S rRNA gene. BMC Res Notes. 2016;9:380. Epub 2016/08/04. doi: 10.1186/s13104-016-2172-6 27485508; PubMed Central PMCID: PMC4970291.

33. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(Database issue):D590–6. Epub 2012/11/30. doi: 10.1093/nar/gks1219 23193283; PubMed Central PMCID: PMC3531112.

34. McNeilly TN, Mitchell MC, Nisbet AJ, McAteer S, Erridge C, Inglis NF, et al. IgA and IgG antibody responses following systemic immunization of cattle with native H7 flagellin differ in epitope recognition and capacity to neutralise TLR5 signalling. Vaccine. 2010;28(5):1412–21. Epub 2009/11/21. doi: 10.1016/j.vaccine.2009.10.148 19925908.

35. McNeilly TN, Naylor SW, Mahajan A, Mitchell MC, McAteer S, Deane D, et al. Escherichia coli O157:H7 colonization in cattle following systemic and mucosal immunization with purified H7 flagellin. Infect Immun. 2008;76(6):2594–602. Epub 2008/03/26. doi: 10.1128/IAI.01452-07 18362130; PubMed Central PMCID: PMC2423056.

36. Thornton AB, Thomson DU, Loneragan GH, Fox JT, Burkhardt DT, Emery DA, et al. Effects of a siderophore receptor and porin proteins-based vaccination on fecal shedding of Escherichia coli O157:H7 in experimentally inoculated cattle. J Food Prot. 2009;72(4):866–9. Epub 2009/05/14. doi: 10.4315/0362-028x-72.4.866 19435240.

37. Vilte DA, Larzabal M, Garbaccio S, Gammella M, Rabinovitz BC, Elizondo AM, et al. Reduced faecal shedding of Escherichia coli O157:H7 in cattle following systemic vaccination with gamma-intimin C(2)(8)(0) and EspB proteins. Vaccine. 2011;29(23):3962–8. Epub 2011/04/12. doi: 10.1016/j.vaccine.2011.03.079 21477674.

38. Majowicz SE, Scallan E, Jones-Bitton A, Sargeant JM, Stapleton J, Angulo FJ, et al. Global incidence of human Shiga toxin-producing Escherichia coli infections and deaths: a systematic review and knowledge synthesis. Foodborne Pathog Dis. 2014;11(6):447–55. Epub 2014/04/23. doi: 10.1089/fpd.2013.1704 24750096; PubMed Central PMCID: PMC4607253.

39. Scallan EG, Patricia M. A, Frederick J. T, V. R, Hoekstra MR. Foodborne Illness Acquired in the United States—Unspecified Agents. Emerging Infectious Diseases. 2011;17(1):16–22. doi: 10.3201/eid1701.091101p2 21192849

40. Hoffmann S, Batz MB, Morris JG Jr. Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. J Food Prot. 2012;75(7):1292–302. doi: 10.4315/0362-028X.JFP-11-417 22980013.

41. Scharff RL. Economic burden from health losses due to foodborne illness in the United States. J Food Prot. 2012;75(1):123–31. Epub 2012/01/10. doi: 10.4315/0362-028X.JFP-11-058 22221364.

42. Wu HJ, Wu E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes. 2012;3(1):4–14. Epub 2012/02/24. doi: 10.4161/gmic.19320 22356853; PubMed Central PMCID: PMC3337124.

43. McNeilly TN, Mitchell MC, Rosser T, McAteer S, Low JC, Smith DG, et al. Immunization of cattle with a combination of purified intimin-531, EspA and Tir significantly reduces shedding of Escherichia coli O157:H7 following oral challenge. Vaccine. 2010;28(5):1422–8. Epub 2009/11/12. doi: 10.1016/j.vaccine.2009.10.076 19903545.

44. Yoshida M, Claypool SM, Wagner JS, Mizoguchi E, Mizoguchi A, Roopenian DC, et al. Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity. 2004;20(6):769–83. Epub 2004/06/11. doi: 10.1016/j.immuni.2004.05.007 15189741.


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