Mid and hindgut transcriptome profiling analysis of Atlantic salmon (Salmon salar) under unpredictable chronic stress.

Signe Dille Løvmo,Simen R Sandve,Tora Bardal,Paul Whatmore,Angelico Madaro,Rolf Erik Olsen,Mari-Ann Ostensen

doi:10.1098/rsos.191480

Abstract

The intestinal epithelium is a selectively permeable barrier for nutrients, electrolytes and water, while maintaining effective protection against pathogens. Combinations of stressors throughout an animal's life, especially in agriculture and aquaculture settings, may affect the regular operativity of this organ with negative consequences for animal welfare. In the current study, we report the effects of a three-week unpredictable chronic stress (UCS) period on the intestinal morphology and transcriptome response of Atlantic salmon (Salmon salar) parr midgut and hindgut. Midgut and hindgut from both control and UCS fish were collected for histology and RNA-sequencing analysis to identify respective changes in the membrane structures and putative genes and pathways responding to UCS. Histological analysis did not show any significant effect on morphometric parameters. In the midgut, 1030 genes were differentially expressed following UCS, resulting in 279 genes which were involved in 13 metabolic pathways, including tissue repair pathways. In the hindgut, following UCS, 591 differentially expressed genes were detected with 426 downregulated and 165 upregulated. A total of 53 genes were related to three pathways. Downregulated genes include cellular senescence pathways, p53 signalling and cytokine–cytokine receptor pathways. The overall results corroborate that salmon parr were at least partly habituating to the UCS treatment. In midgut, the main upregulation was related to cell growth and repair, while in the hindgut there were indications of the activated apoptotic pathway, reduced cell repair and inhibited immune/anti-inflammatory capacity. This may be the trade-off between habituating to UCS and health resilience. This study suggests possible integrated genetic regulatory mechanisms that are tuned when farmed Atlantic salmon parr attempt to cope with UCS.

Highlights

The gut barrier has several significant biological functions and in addition to the primary function of absorbing nutrients, it is an essential barrier between the fish and the external environment, controlling the loss of nutrients and preventing the uptake of noxious substances
While high stocking densities have been reported to reduce goblet cells (GC) in number and size, as well as villi length in channel catfish (Ictalurus punctatus) [17], no such effects were seen in rainbow trout (Oncorhynchus mykiss) [18]
We report the effects of a three-week unpredictable chronic stress (UCS) trial on the intestinal histology and transcriptome response of Atlantic salmon parr midgut and hindgut

Summary

Introduction

The gut barrier has several significant biological functions and in addition to the primary function of absorbing nutrients, it is an essential barrier between the fish and the external environment, controlling the loss of nutrients and preventing the uptake of noxious substances. Emotional and physical acute and chronic stress has been shown to reduce the physical barrier function leading to increased intestinal permeability, functional dyspepsia, irritable bowel syndrome and peptic ulcer disease [4,5,6,7,8]. While high stocking densities have been reported to reduce goblet cells (GC) in number and size, as well as villi length in channel catfish (Ictalurus punctatus) [17], no such effects were seen in rainbow trout (Oncorhynchus mykiss) [18]. These differences are likely a result of species differences and the lack of proper comparative experimental protocols. Sending Japanese Medaka to the international space station resulted in a greater transcriptional change in the gut compared to other organs, while almost no difference was seen in morphology [21]

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