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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Main Authors: Xinmeng Liao, Yawen Lan, Wentao Wang, Jinjin Zhang, Rui Shao, Zhan Yin, Gudmundur H. Gudmundsson, Peter Bergman, Kangsen Mai, Qinghui Ai, Min Wan
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Gut Microbes
Subjects:
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.
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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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