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Gut microbiota mediates the protective role of Lactobacillus plantarum in ameliorating deoxynivalenol-induced apoptosis and intestinal inflammation of broiler chickens.

ABSTRACT: The protection of Lactobacillus plantarum JM113 against deoxynivalenol (DON)-induced apoptosis and intestinal inflammation on the jejunum of broiler chickens and the potential roles of gut microbiota were determined. A total of 144 one-day-old male broilers (Arbor Acres) were randomly divided into 3 treatment groups consisting of 6 replicates with 8 birds per replicate, including the CON (basal diet), the DON (basal diet + 10 mg/kg DON), and the DL (basal diet + 10 mg/kg DON + 1 × 109 CFU/kg L. plantarum JM113). The DON-diet decreased (P < 0.05) the mRNA expression of mucosal defense proteins and mechanistic target of rapamycin pathway genes. Meanwhile, DON challenge significantly increased Bcl-2-associated X gene/B-cell lymphoma 2 gene (Bcl-2) in the jejunum (P < 0.05) and demonstrated proapoptosis status. In contrast, the DL group showed normal immunity-related gene expression of jejunal mucosa and manifested a superior antiapoptosis status. Adding L. plantarum JM113 significantly raised (P < 0.05) propionic acid, n-butyric acid, and total short-chain fatty acids concentrations in cecal contents of birds fed with DON diet. In addition, DON exposure altered bacterial community structure and disturbed the abundance of several bacterial phyla, families, and genera, leading to dysbiosis. Supplementation with JM113 shifted the gut microbiota composition to that of the CON group. Finally, Spearman correlation analysis suggested that most positive correlations with the mRNA expression of immunity-related and apoptosis-regulatory gene were observed within the phylum Bacteroidetes, and most negative correlations with the indicators were observed within the phylum Firmicutes. The mRNA expression of Bcl-2, TLR2, mTOR, Raptor, and RPS6KB1 (P < 0.05), which are regarded as important cell proliferation and antiapoptosis parameters, were significantly negatively associated with the relative abundances of norank_f__Erysipelotrichaceae, Subdoligranulum, and Anaeroplasma, whereas they had a strong positive correlation with Ruminococcaceae_UCG-004, Alistipes, and Ruminococcaceae_NK4A214_group. These results implied that L. plantarum JM113 supplementation could ameliorate DON-induced apoptosis and intestinal inflammation via manipulating the bacterial community composition and could be used as a potential candidate to attenuate intestinal impairments.

SUBMITTER: Yang X

PROVIDER: S-EPMC7597391 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Gut microbiota mediates the protective role of Lactobacillus plantarum in ameliorating deoxynivalenol-induced apoptosis and intestinal inflammation of broiler chickens.

Yang Xin X Liang Saisai S Guo Fangshen F Ren Zhouzheng Z Yang Xiaojun X Long Fangyu F

Poultry science 20200408 5

The protection of Lactobacillus plantarum JM113 against deoxynivalenol (DON)-induced apoptosis and intestinal inflammation on the jejunum of broiler chickens and the potential roles of gut microbiota were determined. A total of 144 one-day-old male broilers (Arbor Acres) were randomly divided into 3 treatment groups consisting of 6 replicates with 8 birds per replicate, including the CON (basal diet), the DON (basal diet + 10 mg/kg DON), and the DL (basal diet + 10 mg/kg DON + 1 × 10<sup>9</sup> ...[more]

PMID: 32359574

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Project description: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-day-old broilers, ileal sIgA 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 bromii (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.

Project description:Dietary deoxynivalenol (DON) impairs the intestinal functions and performance in broiler chickens, whereas little is known about the effect of DON on the gastrointestinal microbiota. This study evaluated the impact of graded levels of dietary DON contamination on the cecal bacterial microbiota, their predicted metabolic abilities and short-chain fatty acid (SCFA) profiles in chickens. In using a single oral lipopolysaccharide (LPS) challenge we further assessed whether an additional intestinal stressor would potentiate DON-related effects on the cecal microbiota. Eighty 1-day-old chicks were fed diets with increasing DON concentrations (0, 2.5, 5, and 10 mg DON per kg diet) for 5 weeks and were sampled after half of the chickens received an oral LPS challenge (1 mg LPS/kg bodyweight) 1 day before sampling. The bacterial composition was investigated by Illumina MiSeq sequencing of the V3-5 region of the 16S rRNA gene. DON-feeding decreased (p < 0.05) the cecal species richness (Chao1) and evenness (Shannon) compared to the non-contaminated diet. The phyla Firmicutes and Proteobacteria tended to linearly increase and decrease with increasing DON-concentrations, respectively. Within the Firmicutes, DON decreased the relative abundance of Oscillospira, Clostridiaceae genus, Clostridium, and Ruminococcaceae genus 2 (p < 0.05), whereas it increased Clostridiales genus 2 (p < 0.05). Moreover, increasing DON levels linearly decreased a high-abundance Enterobacteriaceae genus and an Escherichia/Shigella-OTU (p < 0.05). Changes in the bacterial composition and their imputed metagenomic capabilities may be explained by DON-related changes in host physiology and cecal nutrient availability. The oral LPS challenge only decreased the abundance of an unassigned Clostridiales genus 2 (p = 0.03). Increasing dietary concentrations of DON quadratically increased the cecal total SCFA and butyrate concentration (p < 0.05), whereas a DON × LPS interaction indicated that LPS mainly increased cecal total SCFA, butyrate, and acetate concentrations in chickens fed the diets that were not contaminated with DON. The present findings showed that even the lowest level of dietary DON contamination had modulatory effects on chicken's cecal bacterial microbiota composition and diversity, whereas the additional oral challenge with LPS did not potentiate DON effects on the cecal bacterial composition.

Project description:BACKGROUND:Avian coccidiosis posts a severe threat to poultry production. In addition to commercial attenuated vaccines, other strategies to combat coccidiosis are urgently needed. Lactobacillus plantarum has been frequently used for expression of foreign proteins as an oral vaccine delivery system using traditional erythromycin resistance gene (erm). However, antibiotic selection markers were often used during protein expression and they pose a risk of transferring antibiotic resistance genes to the environment, and significantly restricting the application in field production. Therefore, a food-grade recombinant L. plantarum vaccine candidate would dramatically improve its application potential in the poultry industry. RESULTS:In this study, we firstly replaced the erythromycin resistance gene (erm) of the pLp_1261Inv-derived expression vector with a non-antibiotic, asd-alr fusion gene, yielding a series of non-antibiotic and reliable, food grade expression vectors. In addition, we designed a dual-expression vector that displayed two foreign proteins on the surface of L. plantarum using the anchoring sequences from either a truncated poly-γ-glutamic acid synthetase A (pgsA') from Bacillus subtilis or the L. acidophilus surface layer protein (SlpA). EGFP and mCherry were used as marker proteins to evaluate the surface displayed properties of recombinant L. plantarum strains and were inspected by western blot, flow cytometry and fluorescence microscopy. To further determine its application as oral vaccine candidate, the AMA1 and EtMIC2 genes of E. tenella were anchored on the surface of L. plantarum strain. After oral immunization in chickens, the recombinant L. plantarum strain was able to induce antigen specific humoral, mucosal, and T cell-mediated immune responses, providing efficient protection against coccidiosis challenge. CONCLUSIONS:The novel constructed food grade recombinant L. plantarum strain with double surface displayed antigens provides a potential efficient oral vaccine candidate for coccidiosis.

Project description:BackgroundIntestinal microbiota plays a key role in nutrient digestion and utilization with a profound impact on feed efficiency of livestock animals. However, the intestinal microbes that are critically involved in feed efficiency remain elusive.MethodsTo identify intestinal bacteria associated with residual feed intake (RFI) in chickens, male Cobb broiler chicks were individually housed from day 14 to day 35. Individual RFI values were calculated for 56 chickens. Luminal contents were collected from the ileum, cecum, and cloaca of each animal on day 35. Bacterial DNA was isolated and subjected to 16S rRNA gene sequencing. Intestinal microbiota was classified to the feature level using Deblur and QIIME 2. High and low RFI groups were formed by selecting 15 and 17 chickens with the most extreme RFI values for subsequent LEfSe comparison of the difference in the microbiota. Spearman correlation analysis was further performed to identify correlations between the intestinal microbiota composition and RFI.ResultsNo significant difference in evenness, richness, and overall diversity of the microbiota in the ileum, cecum, or cloaca was observed between high and low RFI chickens. However, LEfSe analysis revealed a number of bacterial features being differentially enriched in either high or low RFI chickens. Spearman correlation analysis further identified many differentially enriched bacterial features to be significantly correlated with RFI (P?<?0.05). Importantly, not all short-chain fatty acid (SCFA) producers showed a positive association with RFI. While two novel members of Oscillibacter and Butyricicoccus were more abundant in low-RFI, high-efficiency chickens, several other SCFA producers such as Subdoligranulum variabile and two related Peptostreptococcaceae members were negatively associated with feed efficiency. Moreover, a few closely-related Lachnospiraceae family members showed a positive correlation with feed efficiency, while others of the same family displayed an opposite relationship.ConclusionsOur results highlight the complexity of the intestinal microbiota and a need to differentiate the bacteria to the species, subspecies, and even strain levels in order to reveal their true association with feed efficiency. Identification of RFI-associated bacteria provides important leads to manipulate the intestinal microbiota for improving production efficiency, profitability, and sustainability of poultry production.

Project description:Coccidiosis is one of the major parasitic diseases in the commercial broiler industry. Probiotics can protect poultry against Eimeria infection. However, the mechanisms are not fully known. Therefore, Lactobacillus plantarum P8 (P8) was used to investigate its anti-coccidial property and mechanism. Five hundred broilers were allocated to five treatments: control diet (NC), control diet + Eimeria infection (IC), control diet containing 1 × 107 cfu/g P8 + Eimeria infection (P8L), control diet containing 1 × 108 cfu/g P8 + Eimeria infection (P8H), and control diet + Eimeria infection + Diclazuril (DIC). At day 14, all treatments except NC were inoculated with sporulated oocysts. Results indicated that Eimeria infection increased the mortality and oocysts shedding, and declined the growth performance as well as the intestinal barrier in Eimeria-treated broilers. On the contrary, dietary supplementation of low level P8, high level P8 and DIC decreased the mortality and oocysts shedding, but improved the growth performance and intestinal barrier. The impaired intestinal morphology in the IC group was also improved by P8H and DIC treatments. Besides, the elevated oxidative stress and pro-inflammation in Eimeria-infected broilers were reduced by P8L, P8H, and DIC treatments. Metagenomic analysis indicated P8 altered the structure of the gut microbiota, and the alteration was more obvious at day 21 than day 42. Notably, IC also increased the abundances of Eimeriidae, Eimeria and Eimeria tenella at day 21, while P8L and DIC decreased the abundances. Correlation analysis revealed that bacteria in Eimeria-treated broilers positively correlated with the intestinal permeability, oxidative stress and inflammation, while bacteria in broilers receiving P8L and DIC negatively correlated with the aforementioned pathological indices. Functional prediction demonstrated that the metagenomes of Eimeria-infected broilers were involved in several diseases. But the metagenomes of P8L-treated broilers were involved in energy metabolism and replication repair. In conclusion, dietary P8 supplementation inhibited oocyst shedding and improved the growth performance as well as the intestinal health of broilers infected with Eimeria, which was closely related to the regulation of gut microbiota. Moreover, the effects of P8 may be more effective in the early infection of coccidia.

Dataset Information

Gut microbiota mediates the protective role of Lactobacillus plantarum in ameliorating deoxynivalenol-induced apoptosis and intestinal inflammation of broiler chickens.

Publications

Gut microbiota mediates the protective role of Lactobacillus plantarum in ameliorating deoxynivalenol-induced apoptosis and intestinal inflammation of broiler chickens.

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