β-Glucan-Induced Immuno-Modulation: A Role for the Intestinal Microbiota and Short-Chain Fatty Acids in Common Carp
Dietary supplementation of fish with β-glucans has been commonly associated with immunomodulation and generally accepted as beneficial for fish health. However, to date the exact mechanisms of immunomodulation by β-glucan supplementation in fish have remained elusive. In mammals, a clear relation be...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-01-01
|
| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.761820/full |
| _version_ | 1828147072400883712 |
|---|---|
| author | Jules Petit Irene de Bruijn Mark R. G. Goldman Erik van den Brink Wilbert F. Pellikaan Maria Forlenza Geert F. Wiegertjes |
| author_facet | Jules Petit Irene de Bruijn Mark R. G. Goldman Erik van den Brink Wilbert F. Pellikaan Maria Forlenza Geert F. Wiegertjes |
| author_sort | Jules Petit |
| collection | DOAJ |
| description | Dietary supplementation of fish with β-glucans has been commonly associated with immunomodulation and generally accepted as beneficial for fish health. However, to date the exact mechanisms of immunomodulation by β-glucan supplementation in fish have remained elusive. In mammals, a clear relation between high-fibre diets, such as those including β-glucans, and diet-induced immunomodulation via intestinal microbiota and associated metabolites has been observed. In this study, first we describe by 16S rRNA sequencing the active naive microbiota of common carp intestine. Based on the abundance of the genus Bacteroides, well known for their capacity to degrade and ferment carbohydrates, we hypothesize that common carp intestinal microbiota could ferment dietary β-glucans. Indeed, two different β-glucan preparations (curdlan and MacroGard®) were both fermented in vitro, albeit with distinct fermentation dynamics and distinct production of short-chain fatty acids (SCFA). Second, we describe the potential immunomodulatory effects of the three dominant SCFAs (acetate, butyrate, and propionate) on head kidney leukocytes, showing effects on both nitric oxide production and expression of several cytokines (il-1b, il-6, tnfα, and il-10) in vitro. Interestingly, we also observed a regulation of expression of several gpr40L genes, which were recently described as putative SCFA receptors. Third, we describe how a single in vivo oral gavage of carp with MacroGard® modulated simultaneously, the expression of several pro-inflammatory genes (il-1b, il-6, tnfα), type I IFN-associated genes (tlr3.1, mx3), and three specific gpr40L genes. The in vivo observations provide indirect support to our in vitro data and the possible role of SCFAs in β-glucan-induced immunomodulation. We discuss how β-glucan-induced immunomodulatory effects can be explained, at least in part, by fermentation of MacroGard® by specific bacteria, part of the naive microbiota of common carp intestine, and how a subsequent production of SFCAs could possibly explain immunomodulation by β-glucan via SCFA receptors present on leukocytes. |
| first_indexed | 2024-04-11T20:55:57Z |
| format | Article |
| id | doaj.art-d1307c8cbe5046ec9fb31696381d66a3 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-11T20:55:57Z |
| publishDate | 2022-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-d1307c8cbe5046ec9fb31696381d66a32022-12-22T04:03:42ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-01-011210.3389/fimmu.2021.761820761820β-Glucan-Induced Immuno-Modulation: A Role for the Intestinal Microbiota and Short-Chain Fatty Acids in Common CarpJules Petit0Irene de Bruijn1Mark R. G. Goldman2Erik van den Brink3Wilbert F. Pellikaan4Maria Forlenza5Geert F. Wiegertjes6Aquaculture and Fisheries Group, Department of Animal Sciences, Wageningen University & Research, Wageningen, NetherlandsDepartment of Microbial Ecology, Netherlands Institute of Ecology-The Royal Netherlands Academy of Arts and Sciences, (NIOO-KNAW), Wageningen, NetherlandsAquaculture and Fisheries Group, Department of Animal Sciences, Wageningen University & Research, Wageningen, NetherlandsAquaculture and Fisheries Group, Department of Animal Sciences, Wageningen University & Research, Wageningen, NetherlandsAnimal Nutrition Group, Department of Animal Sciences, Wageningen University & Research, Wageningen, NetherlandsAquaculture and Fisheries Group, Department of Animal Sciences, Wageningen University & Research, Wageningen, NetherlandsAquaculture and Fisheries Group, Department of Animal Sciences, Wageningen University & Research, Wageningen, NetherlandsDietary supplementation of fish with β-glucans has been commonly associated with immunomodulation and generally accepted as beneficial for fish health. However, to date the exact mechanisms of immunomodulation by β-glucan supplementation in fish have remained elusive. In mammals, a clear relation between high-fibre diets, such as those including β-glucans, and diet-induced immunomodulation via intestinal microbiota and associated metabolites has been observed. In this study, first we describe by 16S rRNA sequencing the active naive microbiota of common carp intestine. Based on the abundance of the genus Bacteroides, well known for their capacity to degrade and ferment carbohydrates, we hypothesize that common carp intestinal microbiota could ferment dietary β-glucans. Indeed, two different β-glucan preparations (curdlan and MacroGard®) were both fermented in vitro, albeit with distinct fermentation dynamics and distinct production of short-chain fatty acids (SCFA). Second, we describe the potential immunomodulatory effects of the three dominant SCFAs (acetate, butyrate, and propionate) on head kidney leukocytes, showing effects on both nitric oxide production and expression of several cytokines (il-1b, il-6, tnfα, and il-10) in vitro. Interestingly, we also observed a regulation of expression of several gpr40L genes, which were recently described as putative SCFA receptors. Third, we describe how a single in vivo oral gavage of carp with MacroGard® modulated simultaneously, the expression of several pro-inflammatory genes (il-1b, il-6, tnfα), type I IFN-associated genes (tlr3.1, mx3), and three specific gpr40L genes. The in vivo observations provide indirect support to our in vitro data and the possible role of SCFAs in β-glucan-induced immunomodulation. We discuss how β-glucan-induced immunomodulatory effects can be explained, at least in part, by fermentation of MacroGard® by specific bacteria, part of the naive microbiota of common carp intestine, and how a subsequent production of SFCAs could possibly explain immunomodulation by β-glucan via SCFA receptors present on leukocytes.https://www.frontiersin.org/articles/10.3389/fimmu.2021.761820/fullSCFAimmunomodulationfishβ-glucanmicrobiota |
| spellingShingle | Jules Petit Irene de Bruijn Mark R. G. Goldman Erik van den Brink Wilbert F. Pellikaan Maria Forlenza Geert F. Wiegertjes β-Glucan-Induced Immuno-Modulation: A Role for the Intestinal Microbiota and Short-Chain Fatty Acids in Common Carp Frontiers in Immunology SCFA immunomodulation fish β-glucan microbiota |
| title | β-Glucan-Induced Immuno-Modulation: A Role for the Intestinal Microbiota and Short-Chain Fatty Acids in Common Carp |
| title_full | β-Glucan-Induced Immuno-Modulation: A Role for the Intestinal Microbiota and Short-Chain Fatty Acids in Common Carp |
| title_fullStr | β-Glucan-Induced Immuno-Modulation: A Role for the Intestinal Microbiota and Short-Chain Fatty Acids in Common Carp |
| title_full_unstemmed | β-Glucan-Induced Immuno-Modulation: A Role for the Intestinal Microbiota and Short-Chain Fatty Acids in Common Carp |
| title_short | β-Glucan-Induced Immuno-Modulation: A Role for the Intestinal Microbiota and Short-Chain Fatty Acids in Common Carp |
| title_sort | β glucan induced immuno modulation a role for the intestinal microbiota and short chain fatty acids in common carp |
| topic | SCFA immunomodulation fish β-glucan microbiota |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2021.761820/full |
| work_keys_str_mv | AT julespetit bglucaninducedimmunomodulationarolefortheintestinalmicrobiotaandshortchainfattyacidsincommoncarp AT irenedebruijn bglucaninducedimmunomodulationarolefortheintestinalmicrobiotaandshortchainfattyacidsincommoncarp AT markrggoldman bglucaninducedimmunomodulationarolefortheintestinalmicrobiotaandshortchainfattyacidsincommoncarp AT erikvandenbrink bglucaninducedimmunomodulationarolefortheintestinalmicrobiotaandshortchainfattyacidsincommoncarp AT wilbertfpellikaan bglucaninducedimmunomodulationarolefortheintestinalmicrobiotaandshortchainfattyacidsincommoncarp AT mariaforlenza bglucaninducedimmunomodulationarolefortheintestinalmicrobiotaandshortchainfattyacidsincommoncarp AT geertfwiegertjes bglucaninducedimmunomodulationarolefortheintestinalmicrobiotaandshortchainfattyacidsincommoncarp |