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. 2021 Feb 22:12:635333.
doi: 10.3389/fmicb.2021.635333. eCollection 2021.

Supplemental Xylooligosaccharide Modulates Intestinal Mucosal Barrier and Cecal Microbiota in Laying Hens Fed Oxidized Fish Oil

Jian-Min Zhou  1 , Hai-Jun Zhang  1 , Shu-Geng Wu  1 , Kai Qiu  1 , Yu Fu  1 , Guang-Hai Qi  1 , Jing Wang  1
Affiliations

Supplemental Xylooligosaccharide Modulates Intestinal Mucosal Barrier and Cecal Microbiota in Laying Hens Fed Oxidized Fish Oil

Jian-Min Zhou et al. Front Microbiol. .

Abstract

Our previous study indicated that dietary xylooligosaccharide (XOS) supplementation improved feed efficiency, ileal morphology, and nutrient digestibility in laying hens. The objective of this study was to evaluate the mitigative effects of XOS on intestinal mucosal barrier impairment and microbiota dysbiosis induced by oxidized fish oil (OFO) in laying hens. A total of 384 Hy-Line Brown layers at 50 weeks of age were randomly divided into four dietary treatments, including the diets supplemented with 20 g/kg of fresh fish oil (FFO group) or 20 g/kg of oxidized fish oil (OFO group), and the OFO diets with XOS addition at 200 mg/kg (OFO/XOS200 group) or 400 mg/kg (OFO/XOS400 group). Each treatment had eight replicates with 12 birds each. The OFO treatment decreased (P < 0.05) the production performance of birds from 7 to 12 weeks of the experiment, reduced (P < 0.05) ileal mucosal secretory immunoglobulin A (sIgA) content, and increased (P < 0.05) serum endotoxin concentration, as well as downregulated (P < 0.05) mRNA expression of claudin-1 (CLDN1) and claudin-5 (CLDN5) in the ileal mucosa at the end of the experiment. Dietary XOS addition (400 mg/kg) recovered (P < 0.05) these changes and further improved (P < 0.05) ileal villus height (VH) and the villus height-to-crypt depth ratio (VCR). In addition, OFO treatment altered cecal microbial composition of layers, and these alterations were probably involved in OFO-induced ileal mucosal impairment as causes or consequences. Supplemental XOS remodeled cecal microbiota of layers fed the OFO diet, characterized by an elevation in microbial richness and changes in microbial composition, including increases in Firmicutes, Ruminococcaceae, Verrucomicrobia (Akkermansia), Paraprevotella, Prevotella_9, and Oscillospira, along with a decrease in Erysipelatoclostridium. The increased abundance of Verrucomicrobia (Akkermansia) had positive correlations with the improved ileal VH and ileal mucosal expression of CLDN1. The abundance of Erysipelatoclostridium decreased by XOS addition was negatively associated with ileal VH, VCR, ileal mucosal sIgA content, and the relative expression of zonula occludens-2, CLDN1, and CLDN5. Collectively, supplemental XOS alleviated OFO-induced intestinal mucosal barrier dysfunction and performance impairment in laying hens, which could be at least partially attributed to the modulation of gut microbiota.

Keywords: XOS; gut microbiota; intestinal mucosal barrier; laying hen; oxidized fish oil.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Effect of dietary xylooligosaccharide supplementation on ileal barrier of laying hens fed oxidized fish oil. (A,B) Show the secretory immunoglobulin A (sIgA) content of ileal mucosal and the endotoxin concentration in serum, respectively. (C) Shows the gene expressions of zona occludens-2 (ZO2), claudin-1 (CLDN1), and claudin-5 (CLDN5) in the ileal mucosa. Data are presented as the means ± SEM (n = 8). FFO, fresh fish oil diet; OFO, oxidized fish oil diet; OFO/XOS200, oxidized fish oil diet + 200 mg/kg of xylooligosaccharide; OFO/XOS400, oxidized fish oil diet + 400 mg/kg of xylooligosaccharide. Bars with no common letter indicate statistical differences among treatments (P < 0.05).
FIGURE 2
FIGURE 2
Influence of xylooligosaccharide on cecal bacterial alpha diversity of laying hens fed oxidized fish oil. Four different alpha diversity metrics, Shannon and Simpson diversity indices, and Ace and Chao richness estimators, were compared among three groups. FFO, fresh fish oil diet; OFO, oxidized fish oil diet; OFO/XOS400, oxidized fish oil diet + 400 mg/kg xylooligosaccharide. P-values given below each boxplot were estimated by Duncan’s multiple range test. ∗ means P < 0.05.
FIGURE 3
FIGURE 3
Beta-diversity analysis of cecal microbiota among three groups. (A) Principal coordinate analysis (PCoA) based on unweighted UniFrac distance calculated from OTU abundance matrix. The horizontal axis represents the first principal coordinate, and the vertical axis means the second one. (B) Partial least squares discriminant analysis (PLS-DA). The horizontal axis represents the first component of PLS-DA, and the vertical axis means the second one. The percentages in parentheses represent the explanatory values of the principal coordinates or the components for the difference in sample composition. FFO (red circles), fresh fish oil diet; OFO (blue triangles), oxidized fish oil diet; OFO/XOS400 (green rectangles), oxidized fish oil diet + 400 mg/kg xylooligosaccharide.
FIGURE 4
FIGURE 4
Effect of dietary xylooligosaccharide supplementation on cecal microbial composition at different taxonomic levels of laying hens fed oxidized fish oil (A) at phylum level, (B) at class level, (C) at family level, and (D) at genus level. Those abundance below 1% were classified as “others.” The relative abundance value shown in the plot represent the average of eight samples in each group. FFO, fresh fish oil diet; OFO, oxidized fish oil diet; OFO/XOS400, oxidized fish oil diet + 400 mg/kg xylooligosaccharide.
FIGURE 5
FIGURE 5
LEfSe identified the most differentially abundant taxa enriched in cecal microbiota among groups FFO (fresh fish oil diet), OFO (oxidized fish oil diet), and OFO/XOS400 (oxidized fish oil diet + 400 mg/kg xylooligosaccharide). (A) Cladogram generated from LEfSe analysis, where red, blue, and green circles represent taxa of greater abundance of hens in the FFO, OFO, and OFO/XOS400 groups, respectively. Yellow circles mean non-significant differences. The diameters of the circles are proportional to the taxon’s abundance. (B) Histogram of the LDA scores computed for features differentially abundant among FFO (red bars), OFO (blue bars), and OFO/XOS400 (green bars) groups. Species with significant difference that have an LDA score greater than 2.0 are presented. The length of the histogram represents the LDA score, which can be interpreted as the effect size of each differentially abundant feature.
FIGURE 6
FIGURE 6
Correlation matrix between key phylotypes (A at phylum level, B at genus level) and phenotypes in laying hens. VH, villus height; VCR, the villus height-to-crypt depth ratio; GCN, goblet cell number; sIgA, secretory immunoglobulin A; ET, endotoxin; ZO2, zona occludens-2; CLDN1, claudin-1; CLDN5, claudin-5. The depth of colors ranging from blue to red represents the magnitude of correlation. The OTUs were organized according to their Pearson correlation coefficient. Significant correlations are noted by *0.01 < P ≤ 0.05, **0.001 < P ≤ 0.01.
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References

    1. Alam A., Neish A. (2018). Role of gut microbiota in intestinal wound healing and barrier function. Tissue Barriers 6 1–22. - PMC - PubMed
    1. Azzam M. M. M., Dong X. Y., Zou X. T. (2017). Effect of dietary threonine on laying performance and intestinal immunity of laying hens fed low-crude-protein diets during the peak production period. J. Anim. Physiol. Anim. Nutr. 101 e55–e66. - PubMed
    1. Barekatain R., Chrystal P. V., Howarth G. S., Mclaughlan C. J., Gilani S., Nattrass G. S. (2019). Performance, intestinal permeability, and gene expression of selected tight junction proteins in broiler chickens fed reduced protein diets supplemented with arginine, glutamine, and glycine subjected to a leaky gut model. Poult. Sci. 98 6761–6771. 10.3382/ps/pez393 - DOI - PMC - PubMed
    1. Belkaid Y., Hand T. (2014). Role of the microbiota in immunity and inflammation. Cell 157 121–141. 10.1016/j.cell.2014.03.011 - DOI - PMC - PubMed
    1. Christensen E. G., Licht T. R., Leser T. D., Bahl M. I. (2014). Dietary xylo-oligosaccharide stimulates intestinal Bifidobacteria and Lactobacilli but has limited effect on intestinal integrity in rats. BMC Res. Notes 7:660. 10.1186/1756-0500-7-660 - DOI - PMC - PubMed

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