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. 2024 Aug 23;16(17):2824.
doi: 10.3390/nu16172824.

Cyclic Oligosaccharide-Induced Modulation of Immunoglobulin A Reactivity to Gut Bacteria Contributes to Alterations in the Bacterial Community Structure

Taisei Miyamoto  1 , Takeshi Tsuruta  1 , Mao Teraoka  1 , Tianyang Wang  1 , Naoki Nishino  1
Affiliations

Cyclic Oligosaccharide-Induced Modulation of Immunoglobulin A Reactivity to Gut Bacteria Contributes to Alterations in the Bacterial Community Structure

Taisei Miyamoto et al. Nutrients. .

Abstract

Immunoglobulin A (IgA) is a major gut antibody that coats commensal gut bacteria and contributes to shaping a stable gut bacterial composition. Although previous studies have shown that cyclic oligosaccharides, including cyclic nigerosyl-1,6-nigerose (CNN) and cyclodextrins (CDs, including αCD, βCD, and γCD), alter the gut bacterial composition, it remains unclear whether cyclic oligosaccharides modify the IgA coating of gut bacteria, which relates to cyclic oligosaccharide-induced alteration of the gut bacterial composition. To address this issue, mice were maintained for 12 weeks on diets containing CNN, αCD, βCD, or γCD; the animals' feces were evaluated for their bacterial composition and the IgA coating index (ICI), a measure of the degree of IgA coating of bacteria. We observed that the intake of each cyclic oligosaccharide altered the gut bacterial composition, with changes in the ICI found at both the phylum and genus levels. The ICI for Bacillota, Lachnospiraceae NK4A136 group, UC Lachnospiraceae, and Tuzzerella were significantly and positively correlated with the relative abundance (RA) in total bacteria for these bacteria; in contrast, significant correlations were not seen for other phyla and genera. Our observations suggest that cyclic oligosaccharide-induced modulation of the IgA coating of gut bacteria may partly relate to changes in the community structure of the gut bacteria.

Keywords: cyclic oligosaccharides; gut bacteria; immunoglobulin A.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Quantification of fecal immunoglobulin A (IgA) concentration, proportion of colonic IgA-secreting plasma cells (IgA-PCs), and mRNA expression in the colon of IgA class-switching recombination-related genes. (A) The fecal IgA concentration. (B) Representative flow cytometric results for the detection of colonic IgA-PCs. (C) Proportions of IgA-PCs among the colonic mononuclear lamina propria (LP) cells. (D) Transcript levels of genes including Aldh1a1, Aldh1a2, April, Baff, and Tgfb1. Data are presented as mean ± SEM (n = 6). Following analysis of variance by Bartlett’s test, data were analyzed by two-tailed one-way ANOVA (equal variances) or Kruskal–Wallis test (unequal variances), and then by post hoc multiple comparisons tests, as needed. Values without a shared letter exhibited statistically significant differences (p < 0.05). Abbreviations: CNN: cyclic nigerosyl-1,6-nigerose; CD: cyclodextrin.
Figure 2
Figure 2
Amounts of short-chain fatty acids (SCFAs) in cecal content samples. (A) Cecal content weight. Amounts of (B) acetate, (C) propionate, and (D) butyrate in cecal content samples. Data are presented as mean ± SEM (n = 6). Following analysis of variance by Bartlett’s test, data were analyzed by two-tailed one-way ANOVA (equal variances) or Kruskal–Wallis test (unequal variances), and then by post hoc multiple comparisons tests, as needed. Values without a shared letter exhibited statistically significant differences (p < 0.05). Abbreviations: CNN: cyclic nigerosyl-1,6-nigerose; CD: cyclodextrin.
Figure 3
Figure 3
Analysis of alpha- and beta-diversity. Alpha-diversity analysis included (A) Shannon diversity and (B) Pielou’s evenness indices of the bacterial community. (C) Beta-diversity analysis using principal coordinate analysis based on unweighted UniFrac distance. Data are presented as median (interquartile range) (n = 6). The Shapiro–Wilk test was applied to test for normality. For data that failed the normality test, differences among groups were evaluated using the two-tailed Kruskal–Wallis test. For data that passed the normality test, equality of variance was tested using Bartlett’s test. Based on the results of Bartlett’s test, differences among groups were evaluated using two-tailed one-way ANOVA (equal variances) or Kruskal–Wallis test (unequal variances), and then by post hoc multiple comparisons tests, as needed. Values without a shared letter exhibited statistically significant differences (p < 0.05). Abbreviations: CNN: cyclic nigerosyl-1,6-nigerose; CD: cyclodextrin.
Figure 4
Figure 4
Correlation between the relative abundance (RA) of total bacteria and the immunoglobulin A (IgA) coating index (ICI). The Shapiro–Wilk test was applied to test for normality. For data that passed the normality test, correlations were assessed using Pearson’s correlation test. For data that failed the normality test, correlations were assessed using Spearman’s correlation test. The phyla and genera that exhibited significant correlations are shown. Abbreviations: CNN: cyclic nigerosyl-1,6-nigerose; CD: cyclodextrin.
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