Effect of dietary histamine on intestinal morphology, inflammatory status, and gut microbiota in yellow catfish (Pelteobagrus fulvidraco)

doi:10.1016/j.fsi.2021.07.017

Fish & Shellfish Immunology

Volume 117, October 2021, Pages 95-103

https://doi.org/10.1016/j.fsi.2021.07.017 Get rights and content

Highlights

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Dietary histamine caused severe abnormality and damage to the intestine.
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Dietary histamine effected the expression of inflammatory genes.
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Dietary histamine altered the gut microbiota composition and diversity.
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Three key gut microbiota bacterial taxa might reduce inflammation.

Abstract

The toxic effect of dietary histamine on the intestine of aquatic animals has been demonstrated, but reports on the morphological observation of the intestine are limited. Thus, a feeding trial was conducted to determine the effect of dietary histamine on intestinal histology, inflammatory status and gut microbiota of yellow catfish (Pelteobagrus fulvidraco). Here, we showed that histamine-rich diets caused severe abnormality and damage to the intestine, including a decreased villi length and reduced villi number. In addition, the quantitative real-time PCR (qRT-PCR) demonstrates that histamine-rich diets increased the expression of pro-inflammatory genes (Tnfα, Il1β, and Il8) and decreased the expression of an anti-inflammatory gene (Il10). Furthermore, the alpha-diversity (observed OTUs, Chao1, Shannon and Simpson) and beta-diversity (non-metric multidimensional scaling, with the stress value of 0.17) demonstrated that histamine-rich diets caused alterations in gut microbiota composition and diversity. Co-occurrence networks analysis of the gut microbiota community showed that the histamine influenced the number and the relationship between bacteria species in the phyla of Acidobacteria, Proteobacteria, and Bacteroidetes, which caused the instability of the intestinal microbiota community. Additionally, random forest selected six bacterial species as the biomarkers to separate the three groups, which are Lachnospiraceae Blautia (V520), Bacteroidales S24.7 (V235), Chloroplast Streptophyta (V368), Actinomycetales Streptomycetaceae (V152), Clostridia Clostridiales (V491) and Paraprevotellaceae Prevotella (V245). Finally, Pearson correlation analysis demonstrated that V520, V235, and V491 were negatively correlated with pro-inflammatory factors (Tnfα, Il1β, and Il8) and positively correlated with an anti-inflammatory factor (Il10), which indicated that V520, V235, and V491 might be anti-inflammatory. These findings improved our understanding of the toxic effect of dietary histamine to intestinal histological damage, the induction of mucosa inflammatory status, and the alteration of gut microbiota.

Introduction

Histamine is a quality criterion of fish meals as it indicates spoilage [1], which is a threat to food safety as it causes food poisoning in animals. Histamine detection is inevitably produced from the rich histidine in miscellaneous fish and fish meal by histidine decarboxylase-produced bacteria in certain conditions, such as long-distance transport, fish meal preparation in high temperature and bad storage conditions [2,3]. It is well known that histamine content in brown fish meal and inferior fishmeal is much higher than that in white fish meal [4,5], so brown fish meal and inferior fishmeal used in aquaculture may greatly increase the level of dietary histamine in diets. With the global shortage and increasing price of fish meal, brown fish meal and inferior fishmeal have been used partly to replace part of costly white fish meal, which means that histamine will become a great threat to the health of aquatic animals.

A previous study has demonstrated that dietary histamine (1–10 g/kg) causes erosion, necrosis and edema of mucosal epithelium and also necrosis of gastric gland cells in the stomach of rainbow trout (Oncorhynchus mykiss) [6]. When fed with diets supplemented with histamine at 2 g/kg, a decline in feed consumption in the rainbow trout occurred [7]. In recent years, a study reported that inferior fishmeal and miscellaneous fish containing histamine (1–4 g/kg) lead to serious alterations in the hepatopancreas and intestine of Chinese mitten crab [8]. Almost all of the previous studies have focused on the effects of histamine on growth performance and intestinal morphology, but a comprehensive understanding of its impact on intestinal health of aquatic animals remains elusive. Therefore, a moderate level (1 g/kg) and high level (2 g/kg) of dietary histamine were used in the present study to demonstrate the toxic effects on yellow catfish.

The intestine is the most important digestive organ of fish and also plays key roles in metabolism. It has been demonstrated that in multiple aquatic animals, such as crab and grass carp, that different segments of their intestine (foregut, midgut and hindgut) have different histological morphology and physiological function [[8], [9], [10]]. The intestinal mucosal in fish is essential as the primary barrier between the external environment and the closely regulated internal milieu, is essential for fish [11]. Therefore, maintaining a well-functioning intestinal mucosal immune system is of vital importance in maintaining the health of fish. The immunity of the intestine also plays an important role in protecting fish from infection. Nuclear factor-kappa B (NFκB) is a critical transcription factor, which targets a large set of genes associated with immune and defense responses. NFκB is a heterodimer of p50 and p65, which are sequestered in cytosol by IκB. Upon receiving inflammatory signaling, TNF induces the phosphorylation of the IκB protein and triggers its ubiquitination and degradation by the 26s proteasome [12], which leads to the phosphorylation and activation of NFκB and further translocates it into the nucleus. This activates the expression of inflammatory cytokines, such as interleukin (IL)-1β, IL-8, and IL-10, which are secreted from macrophages and monocytes to regulate the host response to infection, mediating different kinds of immune responses [13,14]. In addition, the intestinal microbiota plays a critical role in digestive function and the formation of a defensive barrier to protect the fish against pathogenic invasions. Many factors, such as diets, the species, stages and environmental factors, can modulate the intestinal microbiota community. Meanwhile, the metabolites from different gut microbiota can also affect the host immune system [15,16].

In order to understand precisely the effect of dietary histamine on intestinal histology, inflammatory status and gut microbiota of yellow catfish (Pelteobagrus fulvidraco), the histology of different intestinal segments was observed, the expression of intestinal mucosa inflammatory genes was assessed, and the gut microbiota composition and diversity were analyzed upon dietary histamine supplementation.

Section snippets

Fish and diets

The yellow catfish were purchased from the Guangzhou Yufeng Aquaculture Development Co. Ltd, Guangdong, China. After acclimation for two weeks, the male yellow catfish (10.5 ± 0.6 g initial body weight) were divided equally into 9 tanks with a water volume of approximately 300 L, 40 fish per tank and 3 tanks per group. A basal diet (C0), which served as the control group, was formulated to meet the nutritional requirements of the yellow catfish (Table 1). The other two diets (H1 and H2)

Dietary histamine causes damage to the intestinal morphology of yellow catfish

The structure of the foregut, midgut, and hindgut tissue in the slices is quite different (Fig. 1). As the intestine is closer to the end of the anus, the villi of the intestine become shorter. Unlike the villi of the foregut and midgut, the villi of the hindgut were bifurcated. In addition, the histological phenotypes of foregut, midgut and hindgut indicated that the histamine in diets lead to severe abnormality and damage to the intestine morphology. The villi of the foregut showed a

Discussion

Intestines with a large surface area that acts as a barrier, which are associated with structural integrity, microbiota homeostasis and immunological status [25]. If the structural integrity of the intestine is damaged, pathogens could penetrate the intestine epithelium, leading to immune cells infiltration and host inflammatory response [26]. In a previous study, we observed that 1 g/kg histamine in the diet could cause liver inflammation and intestine damage [15], whereas the growth

Author contributions

Conceptualization, L.X.; Methodology, L.X. W.L. B.L. Z.L. Y.Y. G.X. M.H.; Investigation, W.L. L.X.; Writing Original Draft, W.L.; Writing and Review & Editing, W.L. L.X; Funding Acquisition, L.X. Y.Y.

Acknowledgements

This study was supported by grants of ‘GDAS’ Project of Science and Technology Development (Grant No. 2016GDASRC-0202, 2018GDASCX-0102), Guangdong Province Industry-University-Research Collaborative Innovation and Platform Environment Construction Special Project (2017B090901052) and National Natural Science Foundation of China (8187050617).

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¹: These authors contribute equally.

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Effect of dietary histamine on intestinal morphology, inflammatory status, and gut microbiota in yellow catfish (Pelteobagrus fulvidraco)

Highlights

Abstract

Introduction

Section snippets

Fish and diets

Dietary histamine causes damage to the intestinal morphology of yellow catfish

Discussion

Author contributions

Acknowledgements

Food Contr.

Aquaculture

Aquaculture

Comp. Biochem. Physiol. Part A Physiol.

Fish Shellfish Immunol.

Fish Shellfish Immunol.

Aquaculture

Cell

Mol. Immunol.

Aquaculture

Biol. Blood Marrow Transplant.

Histamine content and isolation of histamine-forming bacteria in fish meal and fish soluble concentrate

Fish. Sci.

A survey of marine trash fish and fish meal as aquaculture feed ingredients in Vietnam

Aust. Cent. Int. Agric. Res.

Effect of dietary histidine or histamine on growth and development of stomach erosion in rainbow-trout

Nippon Suisan Gakkaishi

Histamine Effects Feed Acceptability but Not Protein Utilization by Juvenile Rainbow Trout (Oncorhynchus mykiss)

Effect of dietary histamine supplementation on growth, digestive enzyme activities and morphology of intestine and hepatopancreas in the Chinese mitten crab Eriocheir sinensis

SpringerPlus

Biology and Diseases of Grass Carp

Signaling to NF-κB

Genes Dev.

Deoxynivalenol decreased intestinal immune function related to NF-κB and TOR signalling in juvenile grass carp (Ctenopharyngodon idella)

Fish Shellfish Immunol.

Molecular cloning of IL-6, IL-10, IL-11, IFN-ɤ and modulation of pro- and anti-inflammatory cytokines in cobia (Rachycentron canadum) after Photobacterium damselae subsp. piscicida infection

Comp. Biochem. Physiol. B Biochem. Mol. Biol.

Intestinal Transport Mechanisms and Plasma Cortisol Levels during Normal and Out-Of-Season Parr-Smolt Transformation of Atlantic Salmon

Cecal microbiota of Tibetan Chickens from five geographic regions were determined by 16S rRNA sequencing

Microbiol.

FLASH: fast length adjustment of short reads to improve genome assemblies

Bioinformatics

Using QIIME to analyze 16s rRNA gene sequences from microbial communities

Curr. Protoc. Microbiol.

Topographical and temporal diversity of the human skin microbiome

Science

ggplot2: Elegant Graphics for Data Analysis

Package ‘vegan,’ Community Ecol. Packag. Version. 2