Vitamin D influences gut microbiota and acetate production in zebrafish (Danio rerio) to promote intestinal immunity against invading pathogens
ABSTRACTAlthough evidence has shown that vitamin D (VD) influences gut homeostasis, limited knowledge is available how VD regulates intestinal immunity against bacterial infection. In the present study, cyp2r1 mutant zebrafish, lacking the capacity to metabolize VD, and zebrafish fed a diet devoid o...
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Format: | Article |
Language: | English |
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Taylor & Francis Group
2023-12-01
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Series: | Gut Microbes |
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Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2023.2187575 |
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author | Xinmeng Liao Yawen Lan Wentao Wang Jinjin Zhang Rui Shao Zhan Yin Gudmundur H. Gudmundsson Peter Bergman Kangsen Mai Qinghui Ai Min Wan |
author_facet | Xinmeng Liao Yawen Lan Wentao Wang Jinjin Zhang Rui Shao Zhan Yin Gudmundur H. Gudmundsson Peter Bergman Kangsen Mai Qinghui Ai Min Wan |
author_sort | Xinmeng Liao |
collection | DOAJ |
description | ABSTRACTAlthough evidence has shown that vitamin D (VD) influences gut homeostasis, limited knowledge is available how VD regulates intestinal immunity against bacterial infection. In the present study, cyp2r1 mutant zebrafish, lacking the capacity to metabolize VD, and zebrafish fed a diet devoid of VD, were utilized as VD-deficient animal models. Our results confirmed that the expression of antimicrobial peptides (AMPs) and IL-22 was restrained and the susceptibility to bacterial infection was increased in VD-deficient zebrafish. Furthermore, VD induced AMP expression in zebrafish intestine by activating IL-22 signaling, which was dependent on the microbiota. Further analysis uncovered that the abundance of the acetate-producer Cetobacterium in VD-deficient zebrafish was reduced compared to WT fish. Unexpectedly, VD promoted the growth and acetate production of Cetobacterium somerae under culture in vitro. Importantly, acetate treatment rescued the suppressed expression of β-defensins in VD-deficient zebrafish. Finally, neutrophils contributed to VD-induced AMP expression in zebrafish. In conclusion, our study elucidated that VD modulated gut microbiota composition and production of short-chain fatty acids (SCFAs) in zebrafish intestine, leading to enhanced immunity. |
first_indexed | 2024-03-11T14:20:05Z |
format | Article |
id | doaj.art-1b693eba75194e52aa296d1bb0de5421 |
institution | Directory Open Access Journal |
issn | 1949-0976 1949-0984 |
language | English |
last_indexed | 2024-04-24T17:06:54Z |
publishDate | 2023-12-01 |
publisher | Taylor & Francis Group |
record_format | Article |
series | Gut Microbes |
spelling | doaj.art-1b693eba75194e52aa296d1bb0de54212024-03-28T22:38:20ZengTaylor & Francis GroupGut Microbes1949-09761949-09842023-12-0115110.1080/19490976.2023.2187575Vitamin D influences gut microbiota and acetate production in zebrafish (Danio rerio) to promote intestinal immunity against invading pathogensXinmeng Liao0Yawen Lan1Wentao Wang2Jinjin Zhang3Rui Shao4Zhan Yin5Gudmundur H. Gudmundsson6Peter Bergman7Kangsen Mai8Qinghui Ai9Min Wan10Key Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao, ChinaKey Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao, ChinaKey Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao, ChinaKey Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao, ChinaKey Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaDepartment of Laboratory Medicine, Karolinska Institutet, Stockholm, SwedenDepartment of Laboratory Medicine, Karolinska Institutet, Stockholm, SwedenKey Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao, ChinaKey Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao, ChinaKey Laboratory of Aquaculture Nutrition and Feed, Ministry of Agriculture & Key Laboratory of Mariculture, Ministry of Education, College of Fisheries, Ocean University of China, Qingdao, ChinaABSTRACTAlthough evidence has shown that vitamin D (VD) influences gut homeostasis, limited knowledge is available how VD regulates intestinal immunity against bacterial infection. In the present study, cyp2r1 mutant zebrafish, lacking the capacity to metabolize VD, and zebrafish fed a diet devoid of VD, were utilized as VD-deficient animal models. Our results confirmed that the expression of antimicrobial peptides (AMPs) and IL-22 was restrained and the susceptibility to bacterial infection was increased in VD-deficient zebrafish. Furthermore, VD induced AMP expression in zebrafish intestine by activating IL-22 signaling, which was dependent on the microbiota. Further analysis uncovered that the abundance of the acetate-producer Cetobacterium in VD-deficient zebrafish was reduced compared to WT fish. Unexpectedly, VD promoted the growth and acetate production of Cetobacterium somerae under culture in vitro. Importantly, acetate treatment rescued the suppressed expression of β-defensins in VD-deficient zebrafish. Finally, neutrophils contributed to VD-induced AMP expression in zebrafish. In conclusion, our study elucidated that VD modulated gut microbiota composition and production of short-chain fatty acids (SCFAs) in zebrafish intestine, leading to enhanced immunity.https://www.tandfonline.com/doi/10.1080/19490976.2023.2187575Short-chain fatty acidsmicrobiotavitamin D3antimicrobial peptidesIL-22defensin |
spellingShingle | Xinmeng Liao Yawen Lan Wentao Wang Jinjin Zhang Rui Shao Zhan Yin Gudmundur H. Gudmundsson Peter Bergman Kangsen Mai Qinghui Ai Min Wan Vitamin D influences gut microbiota and acetate production in zebrafish (Danio rerio) to promote intestinal immunity against invading pathogens Gut Microbes Short-chain fatty acids microbiota vitamin D3 antimicrobial peptides IL-22 defensin |
title | Vitamin D influences gut microbiota and acetate production in zebrafish (Danio rerio) to promote intestinal immunity against invading pathogens |
title_full | Vitamin D influences gut microbiota and acetate production in zebrafish (Danio rerio) to promote intestinal immunity against invading pathogens |
title_fullStr | Vitamin D influences gut microbiota and acetate production in zebrafish (Danio rerio) to promote intestinal immunity against invading pathogens |
title_full_unstemmed | Vitamin D influences gut microbiota and acetate production in zebrafish (Danio rerio) to promote intestinal immunity against invading pathogens |
title_short | Vitamin D influences gut microbiota and acetate production in zebrafish (Danio rerio) to promote intestinal immunity against invading pathogens |
title_sort | vitamin d influences gut microbiota and acetate production in zebrafish danio rerio to promote intestinal immunity against invading pathogens |
topic | Short-chain fatty acids microbiota vitamin D3 antimicrobial peptides IL-22 defensin |
url | https://www.tandfonline.com/doi/10.1080/19490976.2023.2187575 |
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