Intestinal toxicity of deoxynivalenol is limited by supplementation with Lactobacillus plantarum JM113 and consequentially altered gut microbiota in broiler chickens
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  • 英文篇名:Intestinal toxicity of deoxynivalenol is limited by supplementation with Lactobacillus plantarum JM113 and consequentially altered gut microbiota in broiler chickens
  • 作者:Shengru ; Wu ; Yanli ; Liu ; Yongle ; Duan ; Fangyuan ; Wang ; Fangshen ; Guo ; Fang ; Yan ; Xiaojun ; Yang ; Xin ; Yang
  • 英文作者:Shengru Wu;Yanli Liu;Yongle Duan;Fangyuan Wang;Fangshen Guo;Fang Yan;Xiaojun Yang;Xin Yang;College of Animal Science and Technology,Northwest A&F University;College of animal science and Technology,Hebei Agricultural University;
  • 英文关键词:Broiler chickens;;Deoxynivalenol;;Gut microbiota;;Lactobacillus plantarum JM113;;mRNA sequencing;;16S rRNA gene sequencing
  • 中文刊名:XMSW
  • 英文刊名:畜牧与生物技术杂志(英文版)
  • 机构:College of Animal Science and Technology,Northwest A&F University;College of animal science and Technology,Hebei Agricultural University;
  • 出版日期:2019-03-15
  • 出版单位:Journal of Animal Science and Biotechnology
  • 年:2019
  • 期:v.10
  • 基金:funded by the National Key R&D Program of China(2018YFD0500600 to Xin Yang);; National Natural Science Foundation of China(No.31402095 to Xin Yang);; the National Key R&D Program of China(2017YFD0500500 to Xiaojun Yang);; the Program for Shaanxi Science&Technology(2017ZDXM-NY-087 to Xin Yang,2017TSCXL-NY-04-04 to Xiaojun Yang)
  • 语种:英文;
  • 页:XMSW201901020
  • 页数:13
  • CN:01
  • ISSN:11-5967/S
  • 分类号:222-234
摘要
Background: Limited research has focused on the effect of Lactobacillus on the intestinal toxicity of deoxynivalenol(DON).The present study was conducted to investigate the role of Lactobacillus plantarum(L.plantarum) JM113 in protecting against the intestinal toxicity caused by DON.Methods: A total of 144 one-day-old healthy Arbor Acres broilers were randomly distributed into 3 treatments,including the CON(basal diet),the DON(extra 10 mg/kg deoxynivalenol),and the DL(extra 1 × 109 CFU/kg L.plantarum JM113 based on DON group) treatments.The growth performance,organ indexes,intestinal morphology,pancreatic digestive enzymes,intestinal secreted immunoglobulin A(sIgA),jejunal transcriptome,and intestinal microbiota were evaluated.Results: Compared with the CON and DL groups,the DON supplementation altered intestinal morphology,especially in duodenum and jejunum,where villi were shorter and crypts were deeper(P < 0.05).Meanwhile,the significantly decreased mRNA expression of jejunal claudin-1 and occludin(P < 0.05),ileal rBAT and jejunal GLUT1 of 21-day-old broilers(P < 0.05),as well as duodenal PepT1 and ileal rBAT of 42-day-old broilers were identified in the DON group.Moreover,supplementation with L.plantarum JM113 could increase duodenal expression of IL-10 and IL-12 of 21-dayold broilers,ileal s IgA of 42-day-old broilers,and the bursa of Fabricius index of 21-day-old broilers.Further jejunal transcriptome proved that the genes related to the intestinal absorption and metabolism were significantly reduced in the DON group but a significant increase when supplemented with extra L.plantarum JM113.Furthermore,the bacteria related to nutrient utilization,including the Proteobacteria,Escherichia,Cc-115(P < 0.05),Lactobacillus and Prevotella(P < 0.1) were all decreased in the DON group.By contrast,supplementation with L.plantarum JM113 increased the relative abundance of beneficial bacterium,including the Bacteroidetes,Roseburia,Anaerofustis,Anaerostipe,and Ruminococcus bromi(P < 0.05).Specifically,the increased abundance of bacteria in the DL group could be proved by the significantly increased caecal content of propionic acid,n-Butyric acid,and total short-chain fatty acid.Conclusions: L.plantarum JM113 enhanced the digestion,absorption,and metabolic functions of the gut when challenged with DON by reducing the injury to intestinal barriers and by increasing the abundance of beneficial bacterium.
        Background: Limited research has focused on the effect of Lactobacillus on the intestinal toxicity of deoxynivalenol(DON).The present study was conducted to investigate the role of Lactobacillus plantarum(L.plantarum) JM113 in protecting against the intestinal toxicity caused by DON.Methods: A total of 144 one-day-old healthy Arbor Acres broilers were randomly distributed into 3 treatments,including the CON(basal diet),the DON(extra 10 mg/kg deoxynivalenol),and the DL(extra 1 × 109 CFU/kg L.plantarum JM113 based on DON group) treatments.The growth performance,organ indexes,intestinal morphology,pancreatic digestive enzymes,intestinal secreted immunoglobulin A(sIgA),jejunal transcriptome,and intestinal microbiota were evaluated.Results: Compared with the CON and DL groups,the DON supplementation altered intestinal morphology,especially in duodenum and jejunum,where villi were shorter and crypts were deeper(P < 0.05).Meanwhile,the significantly decreased mRNA expression of jejunal claudin-1 and occludin(P < 0.05),ileal rBAT and jejunal GLUT1 of 21-day-old broilers(P < 0.05),as well as duodenal PepT1 and ileal rBAT of 42-day-old broilers were identified in the DON group.Moreover,supplementation with L.plantarum JM113 could increase duodenal expression of IL-10 and IL-12 of 21-dayold broilers,ileal s IgA of 42-day-old broilers,and the bursa of Fabricius index of 21-day-old broilers.Further jejunal transcriptome proved that the genes related to the intestinal absorption and metabolism were significantly reduced in the DON group but a significant increase when supplemented with extra L.plantarum JM113.Furthermore,the bacteria related to nutrient utilization,including the Proteobacteria,Escherichia,Cc-115(P < 0.05),Lactobacillus and Prevotella(P < 0.1) were all decreased in the DON group.By contrast,supplementation with L.plantarum JM113 increased the relative abundance of beneficial bacterium,including the Bacteroidetes,Roseburia,Anaerofustis,Anaerostipe,and Ruminococcus bromi(P < 0.05).Specifically,the increased abundance of bacteria in the DL group could be proved by the significantly increased caecal content of propionic acid,n-Butyric acid,and total short-chain fatty acid.Conclusions: L.plantarum JM113 enhanced the digestion,absorption,and metabolic functions of the gut when challenged with DON by reducing the injury to intestinal barriers and by increasing the abundance of beneficial bacterium.
引文
1.Wu Q,Lohrey L,Cramer B,Yuan Z,Humpf HU.Impact of physicochemical parameters on decomposition of deoxynivalenol during extrusion cooking of wheat grits.J Agric Food Chem.2011;59:12480-5.
    2.Tian Y,Tan Y,Liu N,Liao Y,Sun C,Wang S,et al.Functional agents to biologically control deoxynivalenol contamination in cereal grains.Front Microbiol.2016;7:1-8.https://doi.org/10.3389/fmicb.2016.00395.
    3.Awad WA,Aschenbach JR,Setyabudi F,Razzazi-Fazeli E,B?hm J,Zentek J.In vitro effects of deoxynivalenol on small intestinal d-glucose uptake and absorption of deoxynivalenol across the isolated jejunal epithelium of laying hens.Poult Sci.2007;86:15-20.
    4.Weaver AC,See MT,Kim SW.Protective effect of two yeast based feed additives on pigs chronically exposed to deoxynivalenol and zearalenone.Toxins.2014;6:3336-53.
    5.Awad WA,Zentek J.The feed contaminant deoxynivalenol affects the intestinal barrier permeability through inhibition of protein synthesis.Arch Toxicol.2015;89:961-5.
    6.Payros D,Alassane-Kpembi I,Pierron A,Loiseau N,Pinton P,Oswald IP.Toxicology of deoxynivalenol and its acetylated and modified forms.Arch Toxicol.2016;90:2931-57.
    7.Pinton P,Oswald IP.Effect of deoxynivalenol and other type Btrichothecenes on the intestine:a review.Toxins.2014;6:1615-43.
    8.Pestka JJ.Deoxynivalenol:mechanisms of action,human exposure,and toxicological relevance.Arch Toxicol.2010a;84:663-79.
    9.Pestka JJ.Deoxynivalenol-induced proinflammatory gene expression:mechanisms and pathological sequelae.Toxins.2010b;2:1300-17.
    10.Awad WA,Vahjen W,Aschenbach JR,Zentek J.A diet naturally contaminated with the fusarium mycotoxin deoxynivalenol down regulates gene expression of glucose transporters in the intestine of broiler chickens.Livestock Sci.2011;140:72-9.
    11.Broekaert N,Devreese M,van Bergen T,Schauvliege S,De Boevre M,De Saeger S,et al.In vivo contribution of deoxynivalenol-3-β-D-glucoside to deoxynivalenol exposure in broiler chickens and pigs:oral bioavailability,hydrolysis and toxicokinetics.Arch Toxicol.2017;91:699-712.
    12.Donohoe DR,Garge N,Zhang X,Sun W,O'Connell TM,Bunger MK,et al.The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon.Cell Metab.2011;13:517-26.
    13.Yang L,Liu S,Ding J,Dai R,He C,Xu K,et al.Gut microbiota co-microevolution with selection for host humoral immunity.Front Microbiol.2017;8:1243.https://doi.org/10.3389/fmicb.2017.01243.
    14.Round JL,Mazmanian SK.The gut microbiota shapes intestinal immune responses during health and disease.Nat Rev Immunol.2009;9:313-23.
    15.Tremaroli V,B?ckhed F.Functional interactions between the gut microbiota and host metabolism.Nature.2012;489:242-9.
    16.De Filippo C,Cavalieri D,Di Paola M,Ramazzotti M,Poullet JB,Massart S,et al.Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa.Proc Natl Acad Sci U S A.2010;(33):14691-6.
    17.Jeong HG,Kang MJ,Kim HG,Oh DG,Kim JS,Lee SK,et al.Role of intestinal microflora in xenobiotic-induced toxicity.Mol Nutr Food Res.2013;57:84-99.
    18.Robert H,Payros D,Pinton P,Théodorou V,Mercier-Bonin M,Oswald IP.Impact of mycotoxins on the intestine:are mucus and microbiota new targets?J Toxicol Environ Health B.2017;20:249-75.
    19.Liao Y,Peng Z,Chen L,Nüssler AK,Liu L,Yang W.Deoxynivalenol,gut microbiota and immunotoxicity:a potential approach?Food Chem Toxicol.2018;112:342-54.
    20.Weaver AC,See MT,Hansen JA,Kim YB,De Souza AL,Middleton TF,Kim SW.The use of feed additives to reduce the effects of aflatoxin and deoxynivalenol on pig growth,organ health and immune status during chronic exposure.Toxins.2013;5:1261-81.
    21.Gallo A,Giuberti G,Frisvad JC,Bertuzzi T,Nielsen KF.Review on mycotoxin issues in ruminants:occurrence in forages,effects of mycotoxin ingestion on health status and animal performance and practical strategies to counteract their negative effects.Toxins.2015;7:3057-111.
    22.Yang X,Li L,Duan Y,Yang X.Antioxidant activity of Lactobacillus plantarum JM113 in vitro and its protective effect on broiler chickens challenged with deoxynivalenol.J Anim Sci.2017;95:837-46.
    23.Brisbin JT,Gong J,Orouji S,Esufali J,Mallick AI,Parvizi P,et al.Oral treatment of chickens with lactobacilli influences elicitation of immune responses.Clin Vaccine Immunol.2011;18:1447-55.
    24.Feng J,Liu P,Yang X,Zhao X.Screening of immunomodulatory and adhesive lactobacillus with antagonistic activities against Salmonella from fermented vegetables.World J Microb Biot.2015;31:1947-54.
    25.Naghi Shokri A,Ghasemi HA,Taherpour K.Evaluation of Aloe vera and synbiotic as antibiotic growth promoter substitutions on performance,gut morphology,immune responses and blood constitutes of broiler chickens.Anim Sci J.2017;88:306-13.
    26.Vernon SD,Shukla SK,Conradt J,Unger ER,Reeves WC.Analysis of 16s rRNA gene sequences and circulating cell-free DNA from plasma of chronic fatigue syndrome and non-fatigued subjects.BMC Microbiol.2002;2:39.
    27.Mago?T,Salzberg SL.FLASH:fast length adjustment of short reads to improve genome assemblies.Bioinformatics.2011;27:2957-63.
    28.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;7:335-6.
    29.Edgar RC,Haas BJ,Clemente JC,Quince C,Knight R.UCHIME improves sensitivity and speed of chimera detection.Bioinformatics.2011;15:2194-200.
    30.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;21:494-504.
    31.Edgar RC.UPARSE:highly accurate OTU sequences from microbial amplicon reads.Nat Methods.2013;10:996-8.
    32.Wang Q,Garrity GM,Tiedje JM,Cole JR.Naive Bayesian classifier for rapid assignment of r RNA sequences into the new bacterial taxonomy.Appl Environ Microbiol.2007;73:5261-7.
    33.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;72:5069-72.
    34.Langmead B,Salzberg SL.Fast gapped-read alignment with bowtie 2.Nat Methods.2012;9:357-9.
    35.Trapnell C,Pachter L,Salzberg SL.TopHat:discovering splice junctions with RNA-Seq.Bioinformatics.2009;25:1105-11.
    36.Trapnell C,Williams BA,Pertea G,Mortazavi A,Kwan G,Van Baren MJ,et al.Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.Nat Biotechnol.2010;28:511-5.
    37.Young MD,Wakefield MJ,Smyth GK,Oshlack A.Gene ontology analysis for RNA-seq:accounting for selection bias.Genome Biol.2010;11:R14.https://doi.org/10.1186/gb-2010-11-2-r14.
    38.Xie C,Mao X,Huang J,Ding Y,Wu J,Dong S,et al.KOBAS 2.0:a web server for annotation and identification of enriched pathways and diseases.Nucleic Acids Res.2011;39:W316-22.
    39.Livak KJ,Schmittgen TD.Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method.Methods.2001;25:402-8.
    40.Shen YB,Piao XS,Kim SW,Wang L,Liu P,Yoon I,et al.Effects of yeast culture supplementation on growth performance,intestinal health,and immune response of nursery pigs.J Anim Sci.2009;87:2614-24.
    41.Grossmann J.Molecular mechanisms of“detachment-induced apoptosis-Anoikis.Apoptosis.2002;7:247-60.
    42.Polansky O,Sekelova Z,Faldynova M,Sebkova A,Sisak F,Rychlik I.Important metabolic pathways and biological processes expressed by chicken cecal microbiota.Appl Environ Microbiol.2016;82:1569-76.
    43.Stanley D,Geier MS,Chen H,Hughes RJ,Moore RJ.Comparison of fecal and cecal microbiotas reveals qualitative similarities but quantitative differences.BMC Microbiol.2015;15:51.https://doi.org/10.1186/s12866-015-0388-6.
    44.Torok VA,Hughes RJ,Mikkelsen LL,Perez-Maldonado R,Balding K,MacAlpine R,et al.Identification and characterization of potential performance-related gut microbiotas in broiler chickens across various feeding trials.Appl Environ Microbiol.2011;77:5868-78.
    45.Alassane-Kpembi I,Puel O,Pinton P,Cossalter AM,Chou TC,Oswald IP.Co-exposure to low doses of the food contaminants deoxynivalenol and nivalenol has a synergistic inflammatory effect on intestinal explants.Arch Toxicol.2017;91:2677-87.
    46.Pasternak JA,Aiyer VIA,Hamonic G,Beaulieu AD,Columbus DA,Wilson HL.Molecular and physiological effects on the small intestine of weaner pigs following feeding with Deoxynivalenol-contaminated feed.Toxins.2018;10:E40.https://doi.org/10.3390/toxins10010040.
    47.Akbari P,Braber S,Gremmels H,Koelink PJ,Verheijden KAT,Garssen J,et al.Deoxynivalenol:a trigger for intestinal integrity breakdown.FASEB J.2014;28:2414-29.
    48.Maresca M,Mahfoud R,Garmy N,Fantini J.The mycotoxin deoxynivalenol affects nutrient absorption in human intestinal epithelial cells.J Nutr.2002;132:2723-31.
    49.Constanze P,Carsten S,Pere R,Werner K,Patricia BH.Organ damage and hepatic lipid accumulation in carp(cyprinus carpiol.)after feed-borne exposure to the mycotoxin,deoxynivalenol(DON).Toxins.2014;6:756-78.
    50.Awad WA,B?hm J,Razzazi-Fazeli E,Ghareeb K,Zentek J.Effect of addition of a probiotic microorganism to broiler diets contaminated with deoxynivalenol on performance and histological alterations of intestinal villi of broiler chickens.Poult Sci.2006;85:974-9.
    51.D?nicke S,D?ll S.A probiotic feed additive containing spores of Bacillus subtilis and B.Licheniformis does not prevent absorption and toxic effects of the fusarium toxin deoxynivalenol in piglets.Food Chem Toxicol.2010;48:152-8.
    52.Garc?A GR,Payros D,Pinton P,Dogi CA,Laffitte J,Neves M,et al.Intestinal toxicity of deoxynivalenol is limited by lactobacillus rhamnosus RC007 in pig jejunum explants.Arch Toxicol 2018;92:983-993.
    53.Styriak I,Conkova E,Borutova R,Leng L,Mojzisova J.The effect of some lactobacillus strains on deoxynivalenol biodegradation.Nutrition&Food Science.2007;37:457-61.
    54.Turner PC,Wu QK,Piekkola S,Gratz S,Mykk?nen H,El-Nezami H.Lactobacillus rhamnosus strain gg restores alkaline phosphatase activity in differentiating caco-2 cells dosed with the potent mycotoxin deoxynivalenol.Food Chem Toxicol.2008;46:2118-23.https://doi.org/10.1016/j.fct.2008.02.004.
    55.Maidana LG,Gerez J,Pinho F,Garcia S,Apfl B.Lactobacillus plantarum culture supernatants improve intestinal tissue exposed to deoxynivalenol.Exp Toxicol Pathol.2017;69:666-71.https://doi.org/10.1016/j.etp.2017.06.005.
    56.Warth B,Parich A,Bueschl C,Schoefbeck D,Neumann NK,Kluger B,et al.GC-MS based targeted metabolic profiling identifies changes in the wheat metabolome following deoxynivalenol treatment.Metabolomics.2015;11:722-38.
    57.Ezema C.Probiotics in animal production:a review.J Vet Med Anim Health.2013;5:308-16.https://doi.org/10.5897/JVMAH2013.0201.
    58.Desai AR,Links MG,Collins SA,Mansfield GS,Drew MD,Kessel AGV,et al.Effects of plant-based diets on the distal gut microbiome of rainbow trout(oncorhynchus mykiss).Aquaculture.2012;350:134-42.
    59.Apper E,Weissman D,Respondek F,Guyonvarch A,Baron F,Boisot P,et al.Hydrolysed wheat gluten as part of a diet based on animal and plant proteins supports good growth performance of asian seabass(lates calcarifer),without impairing intestinal morphology or microbiota.Aquaculture.2016;453:40-8.
    60.Kaakoush NO.Insights into the role of erysipelotrichaceae in the human host.Frontiers in Cellular&Infection Microbiology.2015;5:84.https://doi.org/10.3389/fcimb.2015.00084.
    61.Lecomte V,Kaakoush NO,Maloney CA,Raipuria M,Huinao KD,Mitchell HM,et al.Changes in gut microbiota in rats fed a high fat diet correlate with obesity-associated metabolic parameters.PLoS One.2015;10:e0126931.https://doi.org/10.1371/journal.pone.0126931.
    62.Dodd D,Moon YH,Swaminathan K,Mackie RI,Cann IK.Transcriptomic analyses of xylan degradation by prevotella bryantii and insights into energy acquisition by xylanolytic bacteroidetes.J Biol Chem.2010;28530261-73.
    63.Chen J,Deng YX,Zhang B,Liu DY,Hui XU.Effect of cla producing lactobacillus on gut immune function in mice.Food Science&Technology.2017;4:7-15.
    64.Wang H,Ni X,Qing X,Zeng D,Luo M,Liu L,et al.Live probiotic lactobacillus johnsonii bs15 promotes growth performance and lowers fat deposition by improving lipid metabolism,intestinal development,and gut microflora in broilers.Front Microbiol.2017;8 https://doi.org/10.3389/fmicb.2017.01073.
    65.Abell GCJ,Cooke CM,Bennett CN,Conlon MA,Mcorist AL.Phylotypes related to ruminococcus bromii are abundant in the large bowel of humans and increase in response to a diet high in resistant starch.FEMS Microbiol Ecol.2010;66:505-15.
    66.Ze X,Duncan SH,Louis P,Flint HJ.Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon.ISME J.2013;6:1535-43.
    67.Thomas F,Hehemann JH,Rebuffet E,Czjzek M,Michel G.Environmental and gut bacteroidetes:the food connection.Front Microbiol.2011;2:93.https://doi.org/10.3389/fmicb.2011.00093.
    68.Stanley D,Geier MS,Denman SE,Haring VR,Crowley TM,Hughes RJ,et al.Identification of chicken intestinal microbiota correlated with the efficiency of energy extraction from feed.Vet Microbiol.2013;164:85-92.
    69.Louis P,Young P,Holtrop G,Flint HJ.Diversity of human colonic butyrateproducing bacteria revealed by analysis of the butyryl-coa:acetate coatransferase gene.Environ Microbiol.2010;12:304-14.
    70.Sh PSD,Hold GL,Stewart CS,Flint HJ.The microbiology of butyrate formation in the human colon.FEMS Microbiol Lett.2002;217:133-9.

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