Integrative Transcriptomic and microRNAomic Profiling Reveals Immune Mechanism for the Resilience to Soybean Meal Stress in Fish Gut and Liver

Abstract

In aquafeeds, fish-meal has been commonly replaced with plant protein, which often causes enteritis. Currently, foodborne enteritis has few solutions in regards to prevention or cures. The recovery mechanism from enteritis in herbivorous fish may further help understand prevention or therapy. However, few reports could be found regarding the recovery or resilience to fish foodborne enteritis. In this study, grass carp was used as an animal model for soybean meal induced enteritis and it was found that the fish could adapt to the soybean meal at a moderate level of substitution. Resilience to soybean meal stress was found in the 40% soybean meal group for juvenile fish at growth performance, morphological and gene expression levels, after a 7-week feeding trial. Furthermore, the intestinal transcriptomic data, including transcriptome and miRNAome, was applied to demonstrate resilience mechanisms. The result of this study revealed that in juvenile grass carp after a 7-week feeding cycle with 40% soybean meal, the intestine recovered via enhancing both an immune tolerance and wound healing, the liver gradually adapted via re-balancing immune responses, such as phagosome and complement cascades. Also, many immune factors in the gut and liver were systemically revealed among stages of on-setting, remising, and recovering (or relief). In addition, miRNA regulation played a key role in switching immune states. Thus, the present data systemically demonstrated that the molecular adaptation mechanism of fish gut-liver immunity is involved in the resilience to soybean meal stress.

Dietary Bile Acids Enhance Growth, and Alleviate Hepatic Fibrosis Induced by a High Starch Diet via AKT/FOXO1 and cAMP/AMPK/SREBP1 Pathway in Micropterus salmoides

“…Inflammation are protective responses to eliminate the initial cause of cell injury and initiate tissue repair, in which inflammatory cytokines play vital roles (Karin and Clevers, 2016). Wu et al (2018) found that grass carp showed upregulated pro-inflammatory cytokine (IL17) and anti-inflammatory cytokine (IL10) expression during the wound healing stage whereas all down-regulated in the recovery stage both in liver and gut. Wei et al (2019) also reported that failed inflammatory response is a key reason for the severe damage in spiral valve intestine of Amur sturgeon.…”

Integrative Transcriptomic and Small RNA Sequencing Reveals Immune-Related miRNA–mRNA Regulation Network for Soybean Meal-Induced Enteritis in Hybrid Grouper, Epinephelus fuscoguttatus♀ × Epinephelus lanceolatus♂

“…As a result, soybean meal, which is considered one of the most hopeful candidates for fish meal replacement, can partially or fully replace the fish meal but introduces many anti-nutritional factors. Consequently, fish enteritis induced by plant proteins has become one of the main challenges for sustainable aquaculture (2), and this occurs in a dose-dependent manner (1,3).…”

“…Recently, studies of miRNAome in turbot intestinal function have reported that miRNAs contributed to the intestinal immune responses, preventing host infection, which the potential target genes of differentially expressed miRNAs were involved in multiple functional categories, including the RIG-I signaling pathway, immune defense/evasion, the toll-like receptor signaling pathway, and inflammatory responses (23). Also, it was found via small RNA sequencing that fish diet could affect the expression of intestinal miRNAs and target genes and immune-related pathways, including cell adhesion molecules, ECM-receptor interaction, the apoptosis signaling pathway, cytokine-cytokine receptor, and the VEGF signaling pathway (3,24). However, there has been a lack of investigation of the underlying immune response by combining both transcriptomes and small RNA sequencing, and this requires further elucidation, especially in carnivorous fish.…”

“…At the genomic level, most components associated with T lymphocyte function have been identified in fish, suggesting that gut-associated lymphoid tissue has similar functionalities between fish and mammalian T lymphocytes ( 15 ). At the transcriptomic level, immune-related pathways of fish SBMIE have been gradually reported, showing that cytokine–cytokine receptor interaction, NOD-like receptor interaction, the intestinal immune network for IgA production, and the NF-kB, Jak-STAT, T-cell receptor, and TNF signaling pathways played key roles in response to SBM stress ( 3 , 16 ). Fish meal replacement in fish diet by alternative protein sources could change the fish intestine proteome, including innate immune proteins ( 17 ).…”

Integrative Transcriptomic Analysis Reveals the Immune Mechanism for A CyHV-3-Resistant Common Carp Strain

“…The mRNA samples used for transcriptome sequencing were also subjected to realtime quantitative RT-PCR validation (n = 3), following a previously published protocol [14,16]. After RNA isolation, reverse transcription and quantitative PCR (qPCR) experiments were carried out for 11 genes.…”