PUBLICATION

The Growth-Promoting Effect of Dietary Nucleotides in Fish Is Associated with an Intestinal Microbiota-Mediated Reduction in Energy Expenditure

Authors
Guo, X., Ran, C., Zhang, Z., He, S., Jin, M., Zhou, Z.
ID
ZDB-PUB-170331-6
Date
2017
Source
The Journal of nutrition   147(5): 781-788 (Journal)
Registered Authors
He, Suxu, Ran, Chao, Zhang, Zhen, Zhou, Zhigang
Keywords
Fiaf, inflammation, microbiota, nucleotides, standard metabolic rate
MeSH Terms
  • Angiopoietins/metabolism
  • Animal Husbandry
  • Animal Nutritional Physiological Phenomena
  • Animals
  • Basal Metabolism/drug effects*
  • Cytokines/metabolism
  • Dietary Supplements*
  • Gastrointestinal Microbiome*
  • Inflammation/metabolism
  • Intestines/drug effects*
  • Intestines/metabolism
  • Intestines/microbiology
  • Kidney/drug effects
  • Kidney/metabolism
  • Lipolysis/genetics
  • Liver/drug effects
  • Liver/enzymology
  • Muscles/drug effects
  • Muscles/enzymology
  • Nucleotides/pharmacology*
  • Oxygen Consumption
  • Rest
  • Zebrafish*/metabolism
  • Zebrafish*/microbiology
  • Zebrafish Proteins/metabolism
PubMed
28356434 Full text @ J. Nutr.
Abstract
Background: Nucleotides have been used as functional nutrients to improve the growth and health of animals, including fish. The mechanism involved in the growth-promotion effect of nucleotides is still unclear.Objective: We investigated the bioenergetic mechanism underlying the growth-promotion effect of nucleotides in zebrafish and the associated roles played by the intestinal microbiota.Methods: Larval zebrafish were fed a control or a 0.1% mixed nucleotides-supplemented diet for 2 wk. Standard metabolic rate, the minimal rate of energy expenditure by animals at rest, was evaluated by oxygen consumption with the use of a respirometer. The expressions of fasting-induced adipose factor (Fiaf), inflammatory cytokines, and genes involved in fatty acid (FA) oxidation were tested by quantitative reverse transcriptase-polymerase chain reaction. The intestinal microbiota from the nucleotide-fed fish (NT fish) or control fish was transferred to 3-d postfertilization germ-free zebrafish in which oxygen consumption and expression of cytokines and fiaf were evaluated.Results: Compared with controls, nucleotide supplementation at 0.1% increased the weight and energy gains of zebrafish by 10% and 25%, respectively (P < 0.01). Standard metabolic rate was 28% lower in NT fish than in controls (P < 0.001). Nucleotide supplementation downregulated the inflammatory tone in the head kidney of the fish. Moreover, NT fish had a 51% lower intestinal expression of fiaf than did controls (P < 0.05), which was consistent with decreased expression of key genes involved in FA oxidation [carnitine:palmitoyl transferase 1a (cpt1a) and medium-chain acyl coenzyme A dehydrogenase (mcad)] in liver and muscle. Germ-free zebrafish colonized with microbiota from NT fish had a 25% lower standard metabolic rate than did those colonized by control microbiota (P < 0.01), whereas direct nucleotide feeding of germ-free zebrafish did not affect standard metabolic rate relative to germ-free controls that were not fed nucleotides. Furthermore, germ-free zebrafish colonized with nucleotide microbiota exhibited downregulated inflammatory tone and 33% lower fiaf expression compared with their control microbiota-colonized counterparts.Conclusions: The growth-promoting effect of dietary nucleotides in zebrafish involves 2 intestinal microbiota-mediated mechanisms that result in reduced standard metabolic rate: 1) lower inflammatory tone and 2) reduced FA oxidation associated with increased microbial suppression of intestinal fiaf.
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Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping