Intestinal Cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafish

The capability of carbohydrate utilization in fish is limited compared to mammals. It has scientific and practical significance to improve the ability of fish to use carbohydrates. The efficiency of dietary carbohydrate utilization varies among fish with different feeding habits, which are associate...

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Main Authors: Anran Wang, Zhen Zhang, Qianwen Ding, Yalin Yang, Jérôme Bindelle, Chao Ran, Zhigang Zhou
Format: Article
Language:English
Published: Taylor & Francis Group 2021-01-01
Series:Gut Microbes
Subjects:
Online Access:http://dx.doi.org/10.1080/19490976.2021.1900996
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spelling doaj-951eae7989ea49f2b66f02b98491c5f42021-07-26T12:59:35ZengTaylor & Francis GroupGut Microbes1949-09761949-09842021-01-0113110.1080/19490976.2021.19009961900996Intestinal Cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafishAnran Wang0Zhen Zhang1Qianwen Ding2Yalin Yang3Jérôme Bindelle4Chao Ran5Zhigang Zhou6Department of AgroBioChem/Precision Livestock and Nutrition Unit, AgroBioChem/TERRA, Gembloux Agro-Bio Tech, Liège University (ULiège)Chinese Academy of Agricultural SciencesNorwegian University of Science and TechnologyChinese Academy of Agricultural SciencesDepartment of AgroBioChem/Precision Livestock and Nutrition Unit, AgroBioChem/TERRA, Gembloux Agro-Bio Tech, Liège University (ULiège)Chinese Academy of Agricultural SciencesChinese Academy of Agricultural SciencesThe capability of carbohydrate utilization in fish is limited compared to mammals. It has scientific and practical significance to improve the ability of fish to use carbohydrates. The efficiency of dietary carbohydrate utilization varies among fish with different feeding habits, which are associated with differential intestinal microbiota. In this study, we found that zebrafish fed with omnivorous diet (OD) and herbivorous diet (HD) showed better glucose homeostasis compared with carnivorous diet (CD) fed counterpart and the differential glucose utilization efficiency was attributable to the intestinal microbiota. The commensal bacterium Cetobacterium somerae, an acetate producer, was enriched in OD and HD groups, and administration of C. somerae in both adult zebrafish and gnotobiotic larval zebrafish models resulted in improved glucose homeostasis and increased insulin expression, supporting a causative role of C. somerae enrichment in glucose homeostasis in fish. The enrichment of C. somerae was constantly associated with higher acetate levels, and dietary supplementation of acetate promotes glucose utilization in zebrafish, suggesting a contribution of acetate in the function of C. somerae. Furthermore, we found that the beneficial effect of both acetate and C. somerae on glucose homeostasis was mediated through parasympathetic activation. Overall, this work highlights the existence of a C. somerae-brain axis in the regulation of glucose homeostasis in fish and suggests a role of acetate in mediating the axis function. Our results suggest potential strategies for improvement of fish carbohydrate utilization.http://dx.doi.org/10.1080/19490976.2021.1900996gut microbiotacetobacteriumacetateglucose homeostasiszebrafish
collection DOAJ
language English
format Article
sources DOAJ
author Anran Wang
Zhen Zhang
Qianwen Ding
Yalin Yang
Jérôme Bindelle
Chao Ran
Zhigang Zhou
spellingShingle Anran Wang
Zhen Zhang
Qianwen Ding
Yalin Yang
Jérôme Bindelle
Chao Ran
Zhigang Zhou
Intestinal Cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafish
Gut Microbes
gut microbiota
cetobacterium
acetate
glucose homeostasis
zebrafish
author_facet Anran Wang
Zhen Zhang
Qianwen Ding
Yalin Yang
Jérôme Bindelle
Chao Ran
Zhigang Zhou
author_sort Anran Wang
title Intestinal Cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafish
title_short Intestinal Cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafish
title_full Intestinal Cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafish
title_fullStr Intestinal Cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafish
title_full_unstemmed Intestinal Cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafish
title_sort intestinal cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafish
publisher Taylor & Francis Group
series Gut Microbes
issn 1949-0976
1949-0984
publishDate 2021-01-01
description The capability of carbohydrate utilization in fish is limited compared to mammals. It has scientific and practical significance to improve the ability of fish to use carbohydrates. The efficiency of dietary carbohydrate utilization varies among fish with different feeding habits, which are associated with differential intestinal microbiota. In this study, we found that zebrafish fed with omnivorous diet (OD) and herbivorous diet (HD) showed better glucose homeostasis compared with carnivorous diet (CD) fed counterpart and the differential glucose utilization efficiency was attributable to the intestinal microbiota. The commensal bacterium Cetobacterium somerae, an acetate producer, was enriched in OD and HD groups, and administration of C. somerae in both adult zebrafish and gnotobiotic larval zebrafish models resulted in improved glucose homeostasis and increased insulin expression, supporting a causative role of C. somerae enrichment in glucose homeostasis in fish. The enrichment of C. somerae was constantly associated with higher acetate levels, and dietary supplementation of acetate promotes glucose utilization in zebrafish, suggesting a contribution of acetate in the function of C. somerae. Furthermore, we found that the beneficial effect of both acetate and C. somerae on glucose homeostasis was mediated through parasympathetic activation. Overall, this work highlights the existence of a C. somerae-brain axis in the regulation of glucose homeostasis in fish and suggests a role of acetate in mediating the axis function. Our results suggest potential strategies for improvement of fish carbohydrate utilization.
topic gut microbiota
cetobacterium
acetate
glucose homeostasis
zebrafish
url http://dx.doi.org/10.1080/19490976.2021.1900996
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