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Review
.2023 Sep 19:14:1129250.
doi: 10.3389/fmicb.2023.1129250. eCollection 2023.

Saccharomyces cerevisiae boulardii accelerates intestinal microbiota maturation and is correlated with increased secretory IgA production in neonatal dairy calves

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Review

Saccharomyces cerevisiae boulardii accelerates intestinal microbiota maturation and is correlated with increased secretory IgA production in neonatal dairy calves

Lautaro Rostoll Cangiano et al. Front Microbiol..

Abstract

Neonatal calves have a limited capacity to initiate immune responses due to a relatively immature adaptive immune system, which renders them susceptible to many on-farm diseases. At birth, the mucosal surfaces of the intestine are rapidly colonized by microbes in a process that promotes mucosal immunity and primes the development of the adaptive immune system. In a companion study, our group demonstrated that supplementation of a live yeast probiotic,Saccharomyces cerevisiae boulardii (SCB) CNCM I-1079, to calves from birth to 1 week of age stimulates secretory IgA (sIgA) production in the intestine. The objective of the study was to evaluate how SCB supplementation impacts the intestinal microbiota of one-week-old male calves, and how changes in the bacterial community in the intestine relate to the increase in secretory IgA. A total of 20 calves were randomly allocated to one of two treatments at birth: Control (CON,n = 10) fed at 5 g/d of carrier with no live yeast; and SCB (n = 10) fed at 5 g of live SCB per day (10 × 109 CFU/d). Our study revealed that supplementing calves with SCB from birth to 1 week of age had its most marked effects in the ileum, increasing species richness and phylogenetic diversity in addition to expediting the transition to a more interconnected bacterial community. Furthermore, LEfSe analysis revealed that there were several differentially abundant taxa between treatments and that SCB increased the relative abundance the familyEubacteriaceae,Corynebacteriaceae,Eggerthellaceae,Bacillaceae, andRuminococcaceae. Furthermore, network analysis suggests that SCB promoted a more stable bacterial community and appears to reduce colonization withShigella. Lastly, we observed that the probiotic-driven increase in microbial diversity was highly correlated with the enhanced secretory IgA capacity of the ileum, suggesting that the calf's gut mucosal immune system relies on the development of a stable and highly diverse microbial community to provide the necessary cues to train and promote its proper function. In summary, this data shows that supplementation of SCB promoted establishment of a diverse and interconnected microbiota, prevented colonization ofEscherichia Shigella and indicates a possible role in stimulating humoral mucosal immunity.

Keywords: calf health; immune development; intestinal immunity; microbial colonization; microbiome.

Copyright © 2023 Rostoll Cangiano, Villot, Amorin-Hegedus, Malmuthuge, Gruninger, Guan and Steele.

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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
Alpha diversity index in digesta(A) and mucosa(B) at proximal jejunum, ileum, and colon of calves supplemented (SCB) or not (CON) from birth until 1 week of age withSaccharomyces cerevisiae boulardii CNCM I-1079 at 10 × 109 cfu/d. Species richness and diversity index were measured with three different matrices: Chao1, Shannon index, and Faith phylogenetic diversity (PD index). * Indicates a significant difference between CON and SCB groups (p < 0.05), and ± denotes a tendency for a significant difference between CON and SCB groups (p < 0.10). The lines, boxes, and whiskers in the box plots represent the median, and 25th, and 75th percentiles, and the min-to-max distribution of replicate values, respectively.
Figure 2
Figure 2
Non-Metric Multidimensional Scaling Plots (NMDS) based on unweighted unifrac distances in digesta(A–C) and mucosa(D–F) at proximal jejunum, ileum, and colon, respectively, of calves supplemented (SCB) or not (CON) from birth until 1 week of age withSaccharomyces cerevisiae boulardii CNCM I-1079 at 10 × 109 cfu/d. Analysis of similarity (R = ANOSIM) were used to calculatep-values and to test differences in β-diversity among treatment groups.
Figure 3
Figure 3
The linear discriminant analysis effect size (LEfSe) circular cladogram generated from the ileum digesta of ileum bacterial communities from phylum to genus level identified as discriminating taxa for calves supplemented withSaccharomyces cerevisiae boulardii CNCM I-1079 at 10 × 109 cfu/d from birth to 1 week of age (SCB), and non-supplemented calves (CON).
Figure 4
Figure 4
Relative abundance of discriminating taxa based on the LEfSe analysis at the family level(A), and genus level(B) extracted from the ASV feature table compiled using the SILVA database from calves supplemented withSaccharomyces cerevisiae boulardii CNCM I-1079 at 10 × 109 cfu/d from birth to 1 week of age (SCB), and non-supplemented calves (CON). Relative abundance is presented as box and dot plots. The lines, boxes, and whiskers in the box plots represent the median, and 25th, and 75th percentiles, and the min-to-max distribution of replicate values, respectively. Data were analyzed using the Mann–WhitneyU test. * Indicates a significant difference between CON and SCB groups (p < 0.05).
Figure 5
Figure 5
Co-occurrence network analysis using SPIEC-EASI used to infer the influence ofSaccharomyces cerevisiae boulardii CNCM I-1079 supplementation on the microbial ecological networks in ileum digesta, at the phylum, and genus level. CON = non-supplemented calves at phylum level(A), and at genus level(C); SCB = calves supplemented withSaccharomyces cerevisiae boulardii CNCM I-1079 at 10 × 109 cfu/d from birth to 1 week of age at phylum level(B), and at genus level(D).
Figure 6
Figure 6
Stacked bar charts show the relative contribution of the 10 most important keystone species based on Hub score in ileum digesta within the microbiota of each treatment group (Higher hub score denotes an increased level of interconnectivity within the network). CON = non-supplemented calves(A); SCB = calves supplemented withSaccharomyces cerevisiae boulardii CNCM I-1079 at 10 × 109 cfu/d(B) from birth to 1 week of age.
Figure 7
Figure 7
Short chain fatty acid (SCFA) profile in digesta from proximal jejunum (Prox-Jej), ileum, and colon in response to the supplementation ofSaccharomyces cerevisiae boulardii CNCM I-1079 at 10 × 109 cfu/d (SCB) from birth until 1 week of age or not supplemented calves (CON). Values are means ± SD. * Indicates a significant difference between CON and SCB groups (p < 0.05).
Figure 8
Figure 8
Spearman rank correlations of the relative abundance of the discriminatory taxa obtained in LEfSe in addition to theSaccharomyces cerevisiae gene copy numbers (SCB) in ileum digesta with: secretory IgA concentrations in ileum (sIgA-ileum mg/g DM); concentration of total short chain fatty acids (SCFAs), acetate (μmol/mL), propionate (μmol/mL), and caproate (μmol/mL) measured in ileum; and alpha diversity measures: Chao1, Shannon, Faith phylogenetic diversity (PD). Data is graphically presented in a dot plot heatmap. Strong correlations indicated by large circles and weaker correlations indicated by smaller circles. The scale colors denote whether the correlation is positive (closer to 1, blue circles) or negative (closer to −1, red circles).
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