期刊论文详细信息
BMC Genomics
Early life microbial colonization of the gut and intestinal development differ between genetically divergent broiler lines
Mari A. Smits2  Johanna M. J. Rebel3  Lucia M. T. E. Kaal-Lansbergen2  Freddy M. de Bree3  Alex Bossers3  Stephanie A. Vastenhouw3  Gosse Veninga1  Dirkjan Schokker2 
[1]Cobb Europe BV, Boxmeer, The Netherlands
[2]Wageningen Livestock Research, Wageningen, The Netherlands
[3]Central Veterinary Institute, Lelystad, The Netherlands
关键词: Gene expression;    Microbiota;    Immune;    Chicken;    Gut;   
Others  :  1208961
DOI  :  10.1186/s12864-015-1646-6
 received in 2015-01-28, accepted in 2015-05-20,  发布年份 2015
PDF
【 摘 要 】

Background

Host genetic makeup plays a role in early gut microbial colonization and immune programming. Interactions between gut microbiota and host cells of the mucosal layer are of paramount importance for a proper development of host defence mechanisms. For different livestock species, it has already been shown that particular genotypes have increased susceptibilities towards disease causing pathogens.

The objective of this study was to investigate the impact of genotypic variation on both early microbial colonization of the gut and functional development of intestinal tissue. From two genetically diverse chicken lines intestinal content samples were taken for microbiota analyses and intestinal tissue samples were extracted for gene expression analyses, both at three subsequent time-points (days 0, 4, and 16).

Results

The microbiota composition was significantly different between lines on each time point. In contrast, no significant differences were observed regarding changes in the microbiota diversity between the two lines throughout this study. We also observed trends in the microbiota data at genus level when comparing lines X and Y. We observed that approximately 2000 genes showed different temporal gene expression patterns when comparing line X to line Y. Immunological related differences seem to be only present at day 0, because at day 4 and 16 similar gene expression is observed for these two lines. However, for genes involved in cell cycle related processes the data show higher expression over the whole course of time in line Y in comparison to line X.

Conclusions

These data suggest the genetic background influences colonization of gut microbiota after hatch in combination with the functional development of intestinal mucosal tissue, including the programming of the immune system. The results indicate that genetically different chicken lines have different coping mechanisms in early life to cope with the outside world.

【 授权许可】

   
2015 Schokker et al.; licensee BioMed Central.

【 预 览 】
附件列表
Files Size Format View
20150601022549417.pdf 612KB PDF download
Fig. 5. 85KB Image download
Fig. 4. 28KB Image download
Fig. 3. 40KB Image download
Fig. 2. 41KB Image download
Fig. 1. 14KB Image download
【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

【 参考文献 】
  • [1]Nauta AJ, Ben Amor K, Knol J, Garssen J, van der Beek EM. Relevance of pre- and postnatal nutrition to development and interplay between the microbiota and metabolic and immune systems. Am J Clin Nutr. 2013; 98(2):586S-93.
  • [2]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(7):1578-93.
  • [3]El Aidy S, van Baarlen P, Derrien M, Lindenbergh-Kortleve DJ, Hooiveld G, Levenez F et al.. Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. Mucosal Immunol. 2012; 5(5):567-79.
  • [4]Cahenzli J, Koller Y, Wyss M, Geuking MB, McCoy KD. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe. 2013; 14(5):559-70.
  • [5]Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature. 2012; 489(7415):231-41.
  • [6]Musso G, Gambino R, Cassader M. Interactions between gut microbiota and host metabolism predisposing to obesity and diabetes. Annu Rev Med. 2011; 62:361-80.
  • [7]Velagapudi VR, Hezaveh R, Reigstad CS, Gopalacharyulu P, Yetukuri L, Islam S et al.. The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res. 2010; 51(5):1101-12.
  • [8]Bates JM, Mittge E, Kuhlman J, Baden KN, Cheesman SE, Guillemin K. Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol. 2006; 297(2):374-86.
  • [9]Lutgendorff F, Akkermans LM, Soderholm JD. The role of microbiota and probiotics in stress-induced gastro-intestinal damage. Curr Mol Med. 2008; 8(4):282-98.
  • [10]Swann J, Wang Y, Abecia L, Costabile A, Tuohy K, Gibson G et al.. Gut microbiome modulates the toxicity of hydrazine: a metabonomic study. Mol Biosyst. 2009; 5(4):351-5.
  • [11]Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nature Rev. 2013; 13(11):790-801.
  • [12]Weng M, Walker WA: The role of gut microbiota in programming the immune phenotype. J Dev Orig Health Dis 2013, 4(3):203–14.
  • [13]Apajalahti J, Kettunen A, Graham H. Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. Worlds Poult Sci J. 2004; 60(2):223-32.
  • [14]Brisbin JT, Gong J, Sharif S. Interactions between commensal bacteria and the gut-associated immune system of the chicken. Anim Health Res Rev. 2008; 9(1):101-10.
  • [15]Torok VA, Hughes RJ, Ophel-Keller K, Ali M, MacAlpine R. Influence of different litter materials on cecal microbiota colonization in broiler chickens. Poult Sci. 2009; 88(12):2474-81.
  • [16]Schokker D, Hoekman AJ, Smits MA, Rebel JM. Gene expression patterns associated with chicken jejunal development. Dev Comp Immunol. 2009; 33(11):1156-64.
  • [17]Bar-Shira E, Friedman A. Development and adaptations of innate immunity in the gastrointestinal tract of the newly hatched chick. Dev Comp Immunol. 2006; 30(10):930-41.
  • [18]Bar-Shira E, Sklan D, Friedman A. Establishment of immune competence in the avian GALT during the immediate post-hatch period. Dev Comp Immunol. 2003; 27(2):147-57.
  • [19]Sekelja M, Rud I, Knutsen SH, Denstadli V, Westereng B, Naes T et al.. Abrupt temporal fluctuations in the chicken fecal microbiota are explained by its gastrointestinal origin. Appl Environ Microbiol. 2012; 78(8):2941-8.
  • [20]Stanley D, Geier MS, Hughes RJ, Denman SE, Moore RJ. Highly variable microbiota development in the chicken gastrointestinal tract. PLoS One. 2013; 8(12):e84290.
  • [21]Campbell JH, Foster CM, Vishnivetskaya T, Campbell AG, Yang ZK, Wymore A et al.. Host genetic and environmental effects on mouse intestinal microbiota. ISME J. 2012; 6(11):2033-44.
  • [22]Spor A, Koren O, Ley R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol. 2011; 9(4):279-90.
  • [23]Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J et al.. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci U S A. 2010; 107(44):18933-8.
  • [24]Peterson LW, Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nature Rev. 2014; 14(3):141-53.
  • [25]Forder RE, Howarth GS, Tivey DR, Hughes RJ. Bacterial modulation of small intestinal goblet cells and mucin composition during early posthatch development of poultry. Poult Sci. 2007; 86(11):2396-403.
  • [26]Mulder IE, Schmidt B, Lewis M, Delday M, Stokes CR, Bailey M et al.. Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity. PLoS One. 2011; 6(12):e28279.
  • [27]Schokker D, Zhang J, Zhang LL, Vastenhouw SA, Heilig HG, Smidt H et al.. Early-life environmental variation affects intestinal microbiota and immune development in new-born piglets. PLoS One. 2014; 9(6):e100040.
  • [28]Kelly D, King T, Aminov R. Importance of microbial colonization of the gut in early life to the development of immunity. Mutat Res. 2007; 622(1-2):58-69.
  • [29]Swaggerty CL, Pevzner IY, Lowry VK, Farnell MB, Kogut MH. Functional comparison of heterophils isolated from commercial broiler chickens. Avian Pathol. 2003; 32(1):95-102.
  • [30]Ferro PJ, Swaggerty CL, Kaiser P, Pevzner IY, Kogut MH. Heterophils isolated from chickens resistant to extra-intestinal Salmonella enteritidis infection express higher levels of pro-inflammatory cytokine mRNA following infection than heterophils from susceptible chickens. Epidemiol Infect. 2004; 132(6):1029-37.
  • [31]Swaggerty CL, Ferro PJ, Pevzner IY, Kogut MH. Heterophils are associated with resistance to systemic Salmonella enteritidis infections in genetically distinct chicken lines. FEMS Immunol Med Microbiol. 2005; 43(2):149-54.
  • [32]Swaggerty CL, Lowry VK, Ferro PJ, Pevzner IY, Kogut MH. Disparity in susceptibility to vancomycin-resistant Enterococcus organ invasion in commercial broiler chickens that differ in innate immune responsiveness. Food Agr Immunol. 2005; 16(1):1-15.
  • [33]Li XY, Swaggerty CL, Kogut MH, Chiang HI, Wang Y, Genovese KJ et al.. Systemic response to Campylobacter jejuni infection by profiling gene transcription in the spleens of two genetic lines of chickens. Immunogenetics. 2012; 64(1):59-69.
  • [34]Li X, Swaggerty CL, Kogut MH, Chiang H, Wang Y, Genovese KJ et al.. The paternal effect of Campylobacter jejuni colonization in ceca in broilers. Poult Sci. 2008; 87(9):1742-7.
  • [35]Swaggerty CL, Pevzner IY, Kaiser P, Kogut MH. Profiling pro-inflammatory cytokine and chemokine mRNA expression levels as a novel method for selection of increased innate immune responsiveness. Vet Immunol Immunopathol. 2008; 126(1-2):35-42.
  • [36]Pfefferle PI, Renz H. The mucosal microbiome in shaping health and disease. F1000prime reports. 2014; 6:11.
  • [37]Sommer F, Backhed F. The gut microbiota–masters of host development and physiology. Nat Rev Microbiol. 2013; 11(4):227-38.
  • [38]Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N et al.. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010; 107(26):11971-5.
  • [39]Hildebrand F, Nguyen TL, Brinkman B, Yunta RG, Cauwe B, Vandenabeele P et al.. Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol. 2013; 14(1):R4. BioMed Central Full Text
  • [40]Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R et al.. Human genetics shape the gut microbiome. Cell. 2014; 159(4):789-99.
  • [41]Swaggerty CL, Pevzner IY, Kogut MH. Selection for pro-inflammatory mediators yields chickens with increased resistance against Salmonella enterica serovar Enteritidis. Poult Sci. 2014; 93(3):535-44.
  • [42]Gilmore MS, Lebreton F, van Schaik W. Genomic transition of enterococci from gut commensals to leading causes of multidrug-resistant hospital infection in the antibiotic era. Curr Opin Microbiol. 2013; 16(1):10-6.
  • [43]Mundt JO. Occurrence of enterococci in animals in a wild environment. Appl Microbiol. 1963; 11:136-40.
  • [44]Hollenbeck BL, Rice LB. Intrinsic and acquired resistance mechanisms in enterococcus. Virulence. 2012; 3(5):421-33.
  • [45]Schierack P, Walk N, Reiter K, Weyrauch KD, Wieler LH. Composition of intestinal Enterobacteriaceae populations of healthy domestic pigs. Microbiology. 2007; 153(Pt 11):3830-7.
  • [46]Pascual M, Hugas M, Badiola JI, Monfort JM, Garriga M. Lactobacillus salivarius CTC2197 prevents Salmonella enteritidis colonization in chickens. Appl Environ Microbiol. 1999; 65(11):4981-6.
  • [47]Dalloul RA, Lillehoj HS, Shellem TA, Doerr JA. Enhanced mucosal immunity against Eimeria acervulina in broilers fed a Lactobacillus-based probiotic. Poult Sci. 2003; 82(1):62-6.
  • [48]La Ragione RM, Narbad A, Gasson MJ, Woodward MJ. In vivo characterization of Lactobacillus johnsonii FI9785 for use as a defined competitive exclusion agent against bacterial pathogens in poultry. Lett Appl Microbiol. 2004; 38(3):197-205.
  • [49]Harty DWS, Oakey HJ, Patrikakis M, Hume EBH, Knox KW. Pathogenic potential of lactobacilli. Int J Food Microbiol. 1994; 24(1-2):179-89.
  • [50]Berggren A, Lazou Ahren I, Larsson N, Onning G. Randomised, double-blind and placebo-controlled study using new probiotic lactobacilli for strengthening the body immune defence against viral infections. Eur J Nutr. 2011; 50(3):203-10.
  • [51]Ebrahimi-Mameghani M, Sanaie S, Mahmoodpoor A, Hamishehkar H. Effect of a probiotic preparation (VSL#3) in critically ill patients: a randomized, double-blind, placebo-controlled trial (pilot study). Pak J Med Sci. 2013; 29(2):490-4.
  • [52]Miele E, Pascarella F, Giannetti E, Quaglietta L, Baldassano RN, Staiano A. Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis. Am J Gastroenterol. 2009; 104(2):437-43.
  • [53]Niedzielin K, Kordecki H, Birkenfeld B. A controlled, double-blind, randomized study on the efficacy of Lactobacillus plantarum 299 V in patients with irritable bowel syndrome. Eur J Gastroenterol Hepatol. 2001; 13(10):1143-7.
  • [54]Neal-McKinney JM, Lu X, Duong T, Larson CL, Call DR, Shah DH et al.. Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PLoS One. 2012; 7(9):e43928.
  • [55]Mappley LJ, Tchorzewska MA, Nunez A, Woodward MJ, Bramley PM, La Ragione RM. Oral treatment of chickens with Lactobacillus reuteri LM1 reduces Brachyspira pilosicoli-induced pathology. J Med Microbiol. 2013; 62(Pt 2):287-96.
  • [56]Abudabos AM. Use of a competitive exclusion product (Aviguard (R)) to prevent clostridium perfringens colonization in broiler chicken under induced challenge. Pak J Zool. 2013; 45(2):371-6.
  • [57]Hall PA, Coates PJ, Ansari B, Hopwood D. Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci. 1994; 107(Pt 12):3569-77.
  • [58]Gunther C, Neumann H, Neurath MF, Becker C. Apoptosis, necrosis and necroptosis: cell death regulation in the intestinal epithelium. Gut. 2013; 62(7):1062-71.
  • [59]Yamauchi K, Kamisoyama H, Isshiki Y. Effects of fasting and refeeding on structures of the intestinal villi and epithelial cells in White Leghorn hens. Br Poultry Sci. 1996; 37(5):909-21.
  • [60]Burkholder KM, Thompson KL, Einstein ME, Applegate TJ, Patterson JA. Influence of stressors on normal intestinal microbiota, intestinal morphology, and susceptibility to Salmonella enteritidis colonization in broilers. Poult Sci. 2008; 87(9):1734-41.
  • [61]Teirlynck E, Bjerrum L, Eeckhaut V, Huygebaert G, Pasmans F, Haesebrouck F et al.. The cereal type in feed influences gut wall morphology and intestinal immune cell infiltration in broiler chickens. Brit J Nutr. 2009; 102(10):1453-61.
  • [62]Uni Z, Gal-Garber O, Geyra A, Sklan D, Yahav S. Changes in growth and function of chick small intestine epithelium due to early thermal conditioning. Poult Sci. 2001; 80(4):438-45.
  • [63]Arrieta MC, Bistritz L, Meddings JB. Alterations in intestinal permeability. Gut. 2006; 55(10):1512-20.
  • [64]Turner JR. Intestinal mucosal barrier function in health and disease. Nature Rev. 2009; 9(11):799-809.
  • [65]Keita AV, Soderholm JD. The intestinal barrier and its regulation by neuroimmune factors. Neurogastroenterol Motil. 2010; 22(7):718-33.
  • [66]Camilleri M, Madsen K, Spiller R, Greenwood-Van Meerveld B, Verne GN. Intestinal barrier function in health and gastrointestinal disease. Neurogastroenterol Motil. 2012; 24(6):503-12.
  • [67]Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al.. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7(5):335-6.
  • [68]McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A et al.. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012; 6(3):610-8.
  • [69]DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al.. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006; 72(7):5069-72.
  • [70]Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G et al.. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 2011; 21(3):494-504.
  • [71]Gentleman R, Carey V, Huber W, Irizarry R, Dudoit S, Smyth GK. Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Springer, New York; 2005: p.397-420.
  • [72]Kauffmann A, Gentleman R, Huber W. ArrayQualityMetrics–a bioconductor package for quality assessment of microarray data. Bioinformatics. 2009; 25(3):415-6.
  • [73]Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J et al: Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5(10).
  • [74]Smyth GK: Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3(1):1–25.
  • [75]da Huang W, Sherman BT, Tan Q, Collins JR, Alvord WG, Roayaei J et al.. The DAVID gene functional classification tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol. 2007; 8(9):R183. BioMed Central Full Text
  • [76]Kumar L, M EF. Mfuzz: a software package for soft clustering of microarray data. Bioinformation. 2007; 2(1):5-7.
  • [77]Futschik ME, Carlisle B. Noise-robust soft clustering of gene expression time-course data. J Bioinform Comput Biol. 2005; 3(4):965-88.
  • [78]Conesa A, Nueda MJ, Ferrer A, Talón M. maSigPro: a method to identify significantly differential expression profiles in time-course microarray experiments. Bioinformatics. 2006; 22(9):1096-102.
  文献评价指标  
  下载次数:1次 浏览次数:2次