Mining chicken ileal microbiota for immunomodulatory ... - Nature.com
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Abstract
The gut microbiota makes important contributions to host immune system development and resistance to pathogen infections, especially during early life. However, studies addressing the immunomodulatory functions of gut microbial individuals or populations are limited. In this study, we explore the systemic impact of the ileal microbiota on immune cell development and function of chickens and identify the members of the microbiota involved in immune system modulation. We initially used a time-series design with six time points to prove that ileal microbiota at different succession stages is intimately connected to immune cell maturation. Antibiotics perturbed the microbiota succession and negatively affected immune development, whereas early exposure to the ileal commensal microbiota from more mature birds promoted immune cell development and facilitated pathogen elimination after Salmonella Typhimurium infection, illustrating that early colonization of gut microbiota is an important driver of immune development. Five bacterial strains, Blautia coccoides, Bacteroides xylanisolvens, Fournierella sp002159185, Romboutsia lituseburensis, and Megamonas funiformis, which are closely related to the immune system development of broiler chickens, were then screened out and validated for their immunomodulatory properties. Our results provide insight into poultry immune system–microbiota interactions and also establish a foundation for targeted immunological interventions aiming to combat infectious diseases and promote poultry health and production.
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Data availability
The raw 16S rRNA gene sequencing data of luminal microbiota from the antibiotic-untreated broiler chickens were obtained from NCBI BioProject PRJNA817429 (unpublished data from our own laboratory), and additional raw 16S rRNA gene sequencing data have been deposited in NCBI BioProject PRJNA904673. The genome data have been deposited in NCBI BioProject PRJNA903494 and PRJNA902159. The transcriptome data have been deposited in NCBI BioProject PRJNA904665. Raw datasets used for multicolor flow cytometry and qRT-PCR are available on FigShare (https://doi.org/10.6084/m9.figshare.21825042).
References
Skarp CPA, Hänninen ML, Rautelin HIK. Campylobacteriosis: the role of poultry meat. Clin Microbiol Infect. 2016;22:103–9.
Article CAS PubMed Google Scholar
Qi J, Li X, Zhang W, Wang H, Zhou G, Xu X. Influence of stewing time on the texture, ultrastructure and in vitro digestibility of meat from the yellow-feathered chicken breed. Anim Sci J. 2018;89:474–82.
Article CAS PubMed Google Scholar
Sedeik ME, El-Shall NA, Awad AM, Abd El-Hack ME, Alowaimer AN, Swelum AA. Comparative evaluation of HVT-IBD vector, immune complex, and live IBD vaccines against vvIBDV in commercial broiler chickens with high maternally derived antibodies. Animals. 2019;9:72.
Article PubMed PubMed Central Google Scholar
El-Shall NA, Shewita RS, Abd El-Hack ME, AlKahtane A, Alarifi S, Alkahtani S, et al. Effect of essential oils on the immune response to some viral vaccines in broiler chickens, with special reference to Newcastle disease virus. Poult Sci. 2020;99:2944–54.
Article CAS PubMed PubMed Central Google Scholar
Maron DF, Smith TJS, Nachman KE. Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Glob Health. 2013;9:48.
Article Google Scholar
Favier CF, de Vos WM, Akkermans AD. Development of bacterial and bifidobacterial communities in feces of newborn babies. Anaerobe. 2003;9:219–29.
Article PubMed Google Scholar
Wang S, Ryan CA, Boyaval P, Dempsey EM, Ross RP, Stanton C. Maternal vertical transmission affecting early-life microbiota development. Trends Microbiol. 2020;28:28–45.
Article CAS PubMed Google Scholar
Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005;122:107–18.
Article CAS PubMed Google Scholar
Baumler AJ, Sperandio V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature. 2016;535:85–93.
Article CAS PubMed PubMed Central Google Scholar
Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature. 2016;535:75–84.
Article CAS PubMed Google Scholar
Kim YG, Sakamoto K, Seo SU, Pickard JM, Gillilland MG 3rd, Pudlo NA, et al. Neonatal acquisition of Clostridia species protects against colonization by bacterial pathogens. Science. 2017;356:315–9.
Article CAS PubMed PubMed Central Google Scholar
Chung H, Pamp SJ, Hill JA, Surana NK, Edelman SM, Troy EB, et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell. 2012;149:1578–93.
Article CAS PubMed PubMed Central Google Scholar
Ostman S, Rask C, Wold AE, Hultkrantz S, Telemo E. Impaired regulatory T cell function in germ-free mice. Eur J Immunol. 2006;36:2336–46.
Article PubMed Google Scholar
Tastan C, Karhan E, Zhou W, Fleming E, Voigt AY, Yao X, et al. Tuning of human MAIT cell activation by commensal bacteria species and MR1-dependent T-cell presentation. Mucosal Immunol. 2018;11:1591–605.
Article CAS PubMed PubMed Central Google Scholar
Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;136:485–98.
Article Google Scholar
Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature. 2013;500:232–6.
Article CAS PubMed Google Scholar
Verma R, Lee C, Jeun EJ, Yi J, Kim KS, Ghosh A, et al. Cell surface polysaccharides of Bifidobacterium bifidum induce the generation of Foxp3+ regulatory T cells. Sci Immunol. 2018;3:eaat6975.
Article PubMed Google Scholar
Dibner JJ, Knight CD, Kitchell ML, Atwell CA, Downs AC, Ivey FJ. Early feeding and development of the immune system in neonatal poultry. J Appl Poult Res. 1998;7:425–36.
Article CAS Google Scholar
Khadem A, Soler L, Everaert N, Niewold TA. Growth promotion in broilers by both oxytetracycline and Macleaya cordata extract is based on their anti-inflammatory properties. Br J Nutr. 2014;112:1110–8.
Article CAS PubMed Google Scholar
Pourabedin M, Guan L, Zhao X. Xylo-oligosaccharides and virginiamycin differentially modulate gut microbial composition in chickens. Microbiome. 2015;3:15.
Article PubMed PubMed Central Google Scholar
Varmuzova K, Kubasova T, Davidova-Gerzova L, Sisak F, Havlickova H, Sebkova A, et al. Composition of gut microbiota influences resistance of newly hatched chickens to Salmonella Enteritidis infection. Front Microbiol. 2016;7:957.
Article PubMed PubMed Central Google Scholar
Zhang X, Akhtar M, Chen Y, Ma Z, Liang Y, Shi D, et al. Chicken jejunal microbiota improves growth performance by mitigating intestinal inflammation. Microbiome. 2022;10:107.
Article CAS PubMed PubMed Central Google Scholar
Freeman TC, Ivens A, Baillie JK, Beraldi D, Barnett MW, Dorward D, et al. A gene expression atlas of the domestic pig. BMC Biol. 2012;10:90.
Article PubMed PubMed Central Google Scholar
Mach N, Berri M, Esquerré D, Chevaleyre C, Lemonnier G, Billon Y, et al. Extensive expression differences along porcine small intestine evidenced by transcriptome sequencing. PLoS ONE. 2014;9:e88515.
Article PubMed PubMed Central Google Scholar
Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol. 2003;69:6816–24.
Article CAS PubMed PubMed Central Google Scholar
Oakley BB, Buhr RJ, Ritz CW, Kiepper BH, Berrang ME, Seal BS, et al. Successional changes in the chicken cecal microbiome during 42 days of growth are independent of organic acid feed additives. BMC Vet Res. 2014;10:282.
Article PubMed PubMed Central Google Scholar
Oakley BB, Kogut MH. Spatial and temporal changes in the broiler chicken cecal and fecal microbiomes and correlations of bacterial taxa with cytokine gene expression. Front Vet Sci. 2016;3:11.
Article PubMed PubMed Central Google Scholar
Hu J, Chen L, Tang Y, Xie C, Xu B, Shi M, et al. Standardized preparation for fecal microbiota transplantation in pigs. Front Microbiol. 2018;9:1328.
Article PubMed PubMed Central Google Scholar
Withanage GS, Kaiser P, Wigley P, Powers C, Mastroeni P, Brooks H, et al. Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar typhimurium. Infect Immun. 2004;72:2152–9.
Article CAS PubMed PubMed Central Google Scholar
Beal RK, Wigley P, Powers C, Hulme SD, Barrow PA, Smith AL. Age at primary infection with Salmonella enterica serovar Typhimurium in the chicken influences persistence of infection and subsequent immunity to re-challenge. Vet Immunol Immunopathol. 2004;100:151–64.
Article CAS PubMed Google Scholar
Beal RK, Powers C, Wigley P, Barrow PA, Kaiser P, Smith AL. A strong antigen-specific T-cell response is associated with age and genetically dependent resistance to avian enteric Salmonellosis. Infect Immun. 2005;73:7509–16.
Article CAS PubMed PubMed Central Google Scholar
Kogut MH, Genovese KJ, He HQ, Swaggerty CL, Jiang YW. Modulation of chicken intestinal immune gene expression by small cationic peptides as feed additives during the first week posthatch. Clin Vaccin Immunol. 2013;20:1440–8.
Article CAS Google Scholar
Hoszowski A, Truszczynski M. Prevention of Salmonella typhimurium caecal colonisation by different preparations for competitive exclusion. Comp Immunol Microbiol Infect Dis. 1997;20:111–7.
Article CAS PubMed Google Scholar
Kramer J, Visscher AH, Wagenaar JA, Boonstra-Blom AG, Jeurissen SH. Characterization of the innate and adaptive immunity to Salmonella enteritidis PT1 infection in four broiler lines. Vet Immunol Immunopathol. 2001;79:219–33.
Article CAS PubMed Google Scholar
Kogut MH, Genovese KJ, He H, Li MA, Jiang YW. The effects of the BT/TAMUS 2032 cationic peptides on innate immunity and susceptibility of young chickens to extraintestinal Salmonella enterica serovar Enteritidis infection. Int Immunopharmacol. 2007;7:912–9.
Article CAS PubMed Google Scholar
Crippen TL, Bischoff KM, Lowry VK, Kogut MH. rP33 activates bacterial killing by chicken peripheral blood heterophils. J Food Prot. 2003;66:787–92.
Article PubMed Google Scholar
Rychlik I, Elsheimer-Matulova M, Kyrova K. Gene expression in the chicken caecum in response to infections with non-typhoid Salmonella. Vet Res. 2014;45:119.
Article PubMed PubMed Central Google Scholar
Kashiwagi M, Hosoi J, Lai J-F, Brissette J, Ziegler SF, Morgan BA, et al. Direct control of regulatory T cells by keratinocytes. Nat Immunol. 2017;18:334–43.
Article CAS PubMed PubMed Central Google Scholar
Atarashi K, Tanoue T, Ando M, Kamada N, Nagano Y, Narushima S, et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell. 2015;163:367–80.
Article CAS PubMed PubMed Central Google Scholar
Lécuyer E, Rakotobe S, Lengliné-Garnier H, Lebreton C, Picard M, Juste C, et al. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity. 2014;40:608–20.
Article PubMed Google Scholar
Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017;389:1218–28.
Article PubMed Google Scholar
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;331:337–41.
Article CAS PubMed Google Scholar
Quandt D, Rothe K, Baerwald C, Rossol M. GPRC6A mediates Alum-induced Nlrp3 inflammasome activation but limits Th2 type antibody responses. Sci Rep. 2015;5:16719.
Article CAS PubMed PubMed Central Google Scholar
Blander JM. The comings and goings of MHC class I molecules herald a new dawn in cross-presentation. Immunol Rev. 2016;272:65–79.
Article CAS PubMed PubMed Central Google Scholar
Shirakawa K, Endo J, Kataoka M, Katsumata Y, Yoshida N, Yamamoto T, et al. IL (Interleukin)-10-STAT3-Galectin-3 axis is essential for osteopontin-producing reparative macrophage polarization after myocardial infarction. Circulation. 2018;138:2021–35.
Article CAS PubMed Google Scholar
Hörhold F, Eisel D, Oswald M, Kolte A, Röll D, Osen W, et al. Reprogramming of macrophages employing gene regulatory and metabolic network models. PLoS Comput Biol. 2020;16:e1007657.
Article PubMed PubMed Central Google Scholar
Dillmann C, Mora J, Olesch C, Brüne B, Weigert A. S1PR4 is required for plasmacytoid dendritic cell differentiation. Biol Chem. 2015;396:775–82.
Article CAS ...
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