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The Effect of Xylooligosaccharide, Xylan, and Whole Wheat Bran on the Human Gut Bacteria

Chen, Miao, Liu, Shujun, Imam, Khandaker Md. Sharif Uddin, Sun, Lichao, Wang, Yulu, Gu, Tianyi, Wen, Boting, Xin, Fengjiao·2020·Frontiers in Microbiology
DOI 10.3389/fmicb.2020.568457PMC PMC7794011
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Abstract

Wheat bran is a cereal rich in dietary fibers that have high levels of ferulic acid, which has prebiotic effects on the intestinal microbiota and the host. Herein we explored the effect of xylooligosaccharide, xylan, and whole wheat bran on the human gut bacteria and screened for potential ferulic acid esterase genes. Using in vitro fermentation, we analyzed the air pressure, pH-value, and short-chain fatty acid levels. We also performed 16S rRNA gene and metagenomic sequencing. A Venn diagram analysis revealed that 80% of the core operational taxonomic units (OTUs) were shared among the samples, and most of the xylooligosaccharide treatment core OTUs (319/333 OTUs) were shared with the other two treatments’ core OTUs. A significant difference analysis revealed that the relative abundance of Dorea, Bilophila, and Sulfurovum in wheat bran treatment was higher than that in xylan and xylooligosaccharide treatments. The clusters of orthologous groups of proteins functional composition of all samples was similar to the microbiota composition of the control. Using metagenomic sequencing, we revealed seven genes containing the conserved residues, Gly-X-Ser-X-Gly, and the catalytic triad, Ser-His-Asp, which are thus potential ferulic acid esterase genes. All the results indicate that xylan and/or xylooligosaccharide, the main dietary fibers in wheat bran, plays a major role in in vitro fermentation by the human gut microbiota.

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FIGURE 1 The in vitro fermentation strategy followed by the main methods of analysis.
FIGURE 1 The in vitro fermentation strategy followed by the main methods of analysis.CC BY · PubMed Central
FIGURE 2 The pH of the in vitro fermentation after 24 h. The significance of the differences in pH was calculated by Kruskal–Wallis test; ****P < 0.0001 compared with the control.
FIGURE 2 The pH of the in vitro fermentation after 24 h. The significance of the differences in pH was calculated by Kruskal–Wallis test; ****P < 0.0001 compared with the control.CC BY · PubMed Central
FIGURE 3 The Shannon diversity index of microbial communities under each treatment at 24 h. Significance was determined between WB and CK, X and CK, and XO and CK using Student’s t-test; ***P < 0.001. WB, wheat bran; X, xylan; XO, xylooligosaccharides.
FIGURE 3 The Shannon diversity index of microbial communities under each treatment at 24 h. Significance was determined between WB and CK, X and CK, and XO and CK using Student’s t-test; ***P < 0.001. WB, wheat bran; X, xylan; XO, xylooligosaccharides.CC BY · PubMed Central
FIGURE 4 Phylogenetic tree analysis. On the left is the phylogenetic tree. The different colors of the branches of the phylogenetic tree represent different phyla: red (Bacteroidetes), blue (Firmicutes), green (Actinobacteria), yellow (Proteobacteria), and purple (Fusobacteria). The length of the branch is the evolutionary distance between two species, namely, the degree of species difference. The right histogram shows the average number of reads belonging to different genus in each treatment. WB, wheat bran; X, xylan; XO, xylooligosaccharides.
FIGURE 4 Phylogenetic tree analysis. On the left is the phylogenetic tree. The different colors of the branches of the phylogenetic tree represent different phyla: red (Bacteroidetes), blue (Firmicutes), green (Actinobacteria), yellow (Proteobacteria), and purple (Fusobacteria). The length of the branch is the evolutionary distance between two species, namely, the degree of species difference. The right histogram shows the average number of reads belonging to different genus in each treatment. WB, wheat bran; X, xylan; XO, xylooligosaccharides.CC BY · PubMed Central
FIGURE 5 Venn diagram analysis; the total number of core operational taxonomic units (OTUs) shared and unique. “Size of each list” means the number of core OTUs from each treatment. “Number of elements” means the total number of shared core OTUs by two, three, and four groups or the total number of specific core OTUs in each treatment. Different colors represent different treatments, overlapping parts represent species that are common among multiple treatments, parts that do not overlap represent species that are specific to the treatment, and numbers indicate the number of corresponding species. WB, wheat bran; X, xylan; XO, xylooligosaccharides.
FIGURE 5 Venn diagram analysis; the total number of core operational taxonomic units (OTUs) shared and unique. “Size of each list” means the number of core OTUs from each treatment. “Number of elements” means the total number of shared core OTUs by two, three, and four groups or the total number of specific core OTUs in each treatment. Different colors represent different treatments, overlapping parts represent species that are common among multiple treatments, parts that do not overlap represent species that are specific to the treatment, and numbers indicate the number of corresponding species. WB, wheat bran; X, xylan; XO, xylooligosaccharides.CC BY · PubMed Central
FIGURE 6 Significant difference test between groups. WB, wheat bran; X, xylan; XO, xylooligosaccharides. Using Kruskal–Wallis H-test, the vertical axis represents the species name at the genus level, the column length corresponds to the average relative abundance of the species in each sample group, and the different colors indicate different groupings. The rightmost side is the P-value; 0.01 < ∗P≤0.05, ∗∗P≤0.01, ***P≤0.001.
FIGURE 6 Significant difference test between groups. WB, wheat bran; X, xylan; XO, xylooligosaccharides. Using Kruskal–Wallis H-test, the vertical axis represents the species name at the genus level, the column length corresponds to the average relative abundance of the species in each sample group, and the different colors indicate different groupings. The rightmost side is the P-value; 0.01 < ∗P≤0.05, ∗∗P≤0.01, ***P≤0.001.CC BY · PubMed Central
FIGURE 7 Phylogenetic distribution of the microbiota lineages in the four groups. WB, wheat bran; X, xylan; XO, xylooligosaccharides. The different color nodes represent microbiota communities that are significantly enriched in the corresponding groups and significantly influence the differences between the groups; the pale yellow nodes indicate that the microbial groups either have no significant effect on the different groups or have no significant effect on the differences between groups.
FIGURE 7 Phylogenetic distribution of the microbiota lineages in the four groups. WB, wheat bran; X, xylan; XO, xylooligosaccharides. The different color nodes represent microbiota communities that are significantly enriched in the corresponding groups and significantly influence the differences between the groups; the pale yellow nodes indicate that the microbial groups either have no significant effect on the different groups or have no significant effect on the differences between groups.CC BY · PubMed Central
FIGURE 8 Comparison of the conserved residues, Gly-X-Ser-X-Gly, and the catalytic triplet, Ser-His-Asp. Multiple alignment showing seven novel amino acid sequences with seven known ferulic acid esterase amino acid sequences. The blue asterisk indicates the conserved residues, G-X-S-X-G, and the triangle refers to the catalytic triplet, Ser-His-Asp. The sequences were obtained from Entry ID KX545370 (Lactobacillus amylovorus CGMCC 11056), Entry ID MK640209 (Lactobacillus crispatus S524), Entry ID KJ596484 (Lactobacillus helveticus KCCM 11223), Entry ID KX545371 (Lactobacillus acidophilus CCTCC AB2010208), Entry ID YP_004890534 (Lactobacillus plantarum TMW 1.460), Entry ID KX545372 (Lactobacillus farciminis CCTCC AB2016237), and Entry ID KX545373 (Lactobacillus fermentum CCTCC AB2010204) corresponding to Fae 744, FaeLac, LA, FaeLam, FaeLcr, LhCE, FaeLfe, lp_fae_2016, and FaeLfa.
FIGURE 8 Comparison of the conserved residues, Gly-X-Ser-X-Gly, and the catalytic triplet, Ser-His-Asp. Multiple alignment showing seven novel amino acid sequences with seven known ferulic acid esterase amino acid sequences. The blue asterisk indicates the conserved residues, G-X-S-X-G, and the triangle refers to the catalytic triplet, Ser-His-Asp. The sequences were obtained from Entry ID KX545370 (Lactobacillus amylovorus CGMCC 11056), Entry ID MK640209 (Lactobacillus crispatus S524), Entry ID KJ596484 (Lactobacillus helveticus KCCM 11223), Entry ID KX545371 (Lactobacillus acidophilus CCTCC AB2010208), Entry ID YP_004890534 (Lactobacillus plantarum TMW 1.460), Entry ID KX545372 (Lactobacillus farciminis CCTCC AB2016237), and Entry ID KX545373 (Lactobacillus fermentum CCTCC AB2010204) corresponding to Fae 744, FaeLac, LA, FaeLam, FaeLcr, LhCE, FaeLfe, lp_fae_2016, and FaeLfa.CC BY · PubMed Central

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Metadata

Authors
Chen, M., Liu, S., Imam, K. M. S. U., Sun, L., Wang, Y., Gu, T., Wen, B., & Xin, F.
Venue
Frontiers in Microbiology
Publisher
Frontiers Media SA
Published
2020-12-03
Volume
11
ISSN
1664-302X
DOI
10.3389/fmicb.2020.568457
PMC
PMC7794011
Cited by
18
References
1
Licence
creativecommons.org/licenses/by/4.0/ (vor)

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