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Article

Impact of Yeast-Derived β-Glucans on the Porcine Gut Microbiota and Immune System in Early Life

1
Laboratory of Microbiology, Wageningen University, 6700 EH Wageningen, The Netherlands
2
Host-Microbe Interactomics Group, Wageningen University, 6700 AH Wageningen, The Netherlands
3
Cell Biology and Immunology Group, Wageningen University, 6700 AH Wageningen, The Netherlands
4
Department of Biomolecular Health Sciences, Division of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, 3584 CL Utrecht, The Netherlands
5
Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort 0110, South Africa
6
Research and Development, Trouw Nutrition, 3800 AG Amersfoort, The Netherlands
*
Author to whom correspondence should be addressed.
Authors contributed equally to this work.
Microorganisms 2020, 8(10), 1573; https://doi.org/10.3390/microorganisms8101573
Received: 31 August 2020 / Revised: 7 October 2020 / Accepted: 9 October 2020 / Published: 13 October 2020
(This article belongs to the Special Issue Gut Microbiota Development in Farm Animals)
Piglets are susceptible to infections in early life and around weaning due to rapid environmental and dietary changes. A compelling target to improve pig health in early life is diet, as it constitutes a pivotal determinant of gut microbial colonization and maturation of the host’s immune system. In the present study, we investigated how supplementation of yeast-derived β-glucans affects the gut microbiota and immune function pre- and post-weaning, and how these complex systems develop over time. From day two after birth until two weeks after weaning, piglets received yeast-derived β-glucans or a control treatment orally and were subsequently vaccinated against Salmonella Typhimurium. Faeces, digesta, blood, and tissue samples were collected to study gut microbiota composition and immune function. Overall, yeast-derived β-glucans did not affect the vaccination response, and only modest effects on faecal microbiota composition and immune parameters were observed, primarily before weaning. This study demonstrates that the pre-weaning period offers a ‘window of opportunity’ to alter the gut microbiota and immune system through diet. However, the observed changes were modest, and any long-lasting effects of yeast-derived β-glucans remain to be elucidated. View Full-Text
Keywords: β-glucans; porcine; gastro-intestinal tract; gut microbiota; immune system; early life β-glucans; porcine; gastro-intestinal tract; gut microbiota; immune system; early life
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Figure 1

  • Supplementary File 1:

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  • Externally hosted supplementary file 1
    Doi: 10.4121/12999620
    Description: Table S1. Experimental diets fed during the experimental period. 1HP 300 (Hamlet protein, Horsens, Denmark); 2 Fylax Forte HC-SP (Trouw Nutrition Selko, Tilburg, The Netherlands) 3 Phyzyme XP 5000 TPT (Danisco Animal Nutrition, Marlbourough, UK ) providing 600 FTU 6-phytase per kg feed; 4 Farmix (Trouw Nutrition, Putten, The Netherlands), provided per kg feed: 8000 IU vit A, 2000 IU vit D3, 100 (weaner) or 150 (nursery) IU vit E-acetate, 1.5 mg menadione, 1 mg thiamine mononitrate, 4 mg riboflavin, 1 mg pyridoxine, 30 µg cyanocobalamin, 20 mg niacin, 12 mg pantothenic acid, 300 µg folic acid, 150 mg choline chloride, 50 mg betain.
  • Externally hosted supplementary file 2
    Doi: 10.4121/12999620
    Description: Figure S1. The pH of digesta from four different gut segments (jejunum, ileum, caecum and colon). The pH of digesta was measured on day 27, 44 and 70 of the study. Samples from control animals (circles; ●) and β-glucan treated animals (triangles; ▲) are presented in this figure (n = 8 per group).
  • Externally hosted supplementary file 3
    Doi: 10.4121/12999620
    Description: Figure S2. Gating strategy for the identification of DC subsets following five-color flow cytometry. Antibodies against CD14, CD172a, CADM1 and CD4 in were used to identify DC subsets in PBMCs (A) and MLN cells (B). After doublet discrimination and selection for viable cells, gates were set on cells with high forward and side scatter (large cells). DC subsets (CD14−), were defined as pDC (CD172a+CADM1-CD4+), cDC1 (CD172alowCADM1+CD4− cells) and cDC2 (CD172a+CADM1+CD4−).
  • Externally hosted supplementary file 4
    Doi: 10.4121/12999620
    Description: Figure S3. Gating strategy for the identification of T lymphocytes and NK cells following six-color flow cytometry. Antibodies against CD3, CD8α, TCR-γδ, CD4, FoxP3 and CD25 were used to identify different cell populations in PBMCs (A) and MLN cells (B). After doublet discrimination and selection for viable cells, gates were set on cells with medium/high forward and side scatter to select for lymphocytes and exclude debris. NK cells were defined as CD3-CD8α+, γδ T cells as CD3+TCR-γδ+, CTLs as CD3+TCR-γδ-CD8a+, T helper cells as CD3+TCR-γδ-CD4+, Memory/Activated (Mem./Act.) T cells as CD3+TCR-γδ-CD4+CD8a+ and T regulatory cells (Tregs) as CD3+TCR-γδ-CD4+CD25highFoxp3+.
  • Externally hosted supplementary file 5
    Doi: 10.4121/12999620
    Description: Figure S4. Weighted Unifrac distance-based Principal Response curves (dbPRC) of differences in pre-weaning (A) and post-weaning (B) faecal microbiota composition between β-glucan (black line) and control (reference baseline with zero PRC values) animals. The horizontal axis represents time, and the vertical axis represent PRC score values. Calculations were performed at the genus level, genera with a score lower than -0.2 or higher than 0.2 are shown on the right y-axis. Asterisks represent genera that were significantly differentially abundant.
  • Externally hosted supplementary file 6
    Doi: 10.4121/12999620
    Description: Figure S5. Taxonomic composition of Archaea within the piglet faeces and digesta over time. Data are given as the mean relative abundance at the genus level by sampling time point (d4-70) and by faeces (fcs) or gut segment; jejunum (jej), ileum (ile), caecum (cae). Data includes samples from both treatment groups.
  • Externally hosted supplementary file 7
    Doi: 10.4121/12999620
    Description: Figure S6. Heatmap of the relative abundance of the 35 most prevalent families in faecal samples over time. Each time point includes the means of 16 pens (8 control pens and 8 β-glucan pens).
  • Externally hosted supplementary file 8
    Doi: 10.4121/12999620
    Description: Figure S7. Levels of cytokines IL-10 (A) and TNFα (B) from LPS stimulated MLN cells and Con-A stimulated PBMCs, respectively. MLN cells and PBMCs were stimulated with 1 µg/mL of LPS or 2.5 µg/mL of Con-A for 24 h. Significant differences between treatments are indicated by asterisks (**; P<0.01 and *; P<0.05). Every dot represents a single animal (n = 7 or 8 per group) and error bars represent standard deviations. Statistical analysis was performed for every time point (T-test) and over time (Two-way ANOVA). Data were checked for normal distribution and equal variances and log-transformed when required.
  • Externally hosted supplementary file 9
    Doi: 10.4121/12999620
    Description: Figure S8. Levels of cytokines TNFα (A, C) and IL-10 (B, D) from stimulated MLN cells and PBMCs. MLN cells and PBMCs were stimulated with 10 µg/mL LPS (A, B) or 5 µg/mL Con-A (C, D) for 24 h. Every dot represents a single animal (n = 7 or 8 per group) and error bars represent standard deviations. Statistical analysis was performed for every time point (T-test) and over time (Two-way ANOVA). Data were checked for normal distribution and equal variances and log-transformed when required. No cytokine levels were detected on day 70 (MLN cells) as indicated by n/a.
  • Externally hosted supplementary file 10
    Doi: 10.4121/12999620
    Description: Figure S9. Correlation plot of several study parameters, including physiological parameters (weight and pH), immunological parameters (MLN cell analysis and stimulation assay) and ileal microbiota composition abundances (genus level). This figure only includes data from day 27 of the study. All correlations with an adjusted p-value below 0.05 are shown in the correlation plot. Color intensity is proportional to the correlation coefficient.
MDPI and ACS Style

de Vries, H.; Geervliet, M.; Jansen, C.A.; Rutten, V.P.M.G.; van Hees, H.; Groothuis, N.; Wells, J.M.; Savelkoul, H.F.J.; Tijhaar, E.; Smidt, H. Impact of Yeast-Derived β-Glucans on the Porcine Gut Microbiota and Immune System in Early Life. Microorganisms 2020, 8, 1573. https://doi.org/10.3390/microorganisms8101573

AMA Style

de Vries H, Geervliet M, Jansen CA, Rutten VPMG, van Hees H, Groothuis N, Wells JM, Savelkoul HFJ, Tijhaar E, Smidt H. Impact of Yeast-Derived β-Glucans on the Porcine Gut Microbiota and Immune System in Early Life. Microorganisms. 2020; 8(10):1573. https://doi.org/10.3390/microorganisms8101573

Chicago/Turabian Style

de Vries, Hugo, Mirelle Geervliet, Christine A. Jansen, Victor P.M.G. Rutten, Hubèrt van Hees, Natalie Groothuis, Jerry M. Wells, Huub F.J. Savelkoul, Edwin Tijhaar, and Hauke Smidt. 2020. "Impact of Yeast-Derived β-Glucans on the Porcine Gut Microbiota and Immune System in Early Life" Microorganisms 8, no. 10: 1573. https://doi.org/10.3390/microorganisms8101573

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