Endoplasmic reticulum stress as a key mechanism in stunted growth of seawater rainbow trout (Oncorhynchus mykiss)

Abstract

Background Rainbow trout (Oncorhynchus mykiss) is a salmonid species with a complex life-history. Wild populations are naturally divided into freshwater residents and sea-run migrants. Migrants undergo an energy-demanding adaptation for life in seawater, known as smoltification, while freshwater residents display these changes in an attenuated magnitude and rate. Despite this, in seawater rainbow trout farming all fish are transferred to seawater. Under these circumstances, weeks after seawater transfer, a significant portion of the fish die (around 10%) or experience growth stunting (GS; around 10%), which represents an important profitability and welfare issue. The underlying causes leading to GS in seawater-transferred rainbow trout remain unknown. In this study, we aimed at characterising the GS phenotype in seawater-transferred rainbow trout using untargeted and targeted approaches. To this end, the liver proteome (LC-MS/MS) and lipidome (LC-MS) of GS and fast-growing phenotypes were profiled to identify molecules and processes that are characteristic of the GS phenotype. Moreover, the transcription, abundance or activity of key proteins and hormones related to osmoregulation (Gill Na+, K + –ATPase activity), growth (plasma IGF-I, and liver igf1, igfbp1b, ghr1 and ctsl) and stress (plasma cortisol) were measured using targeted approaches. Results No differences in Gill Na+, K + –ATPase activity and plasma cortisol were detected between the two groups. However, a significant downregulation in plasma IGF-I and liver igf1 transcription pointed at this growth factor as an important pathomechanism for GS. Changes in the liver proteome revealed reactive-oxygen-species-mediated endoplasmic reticulum stress as a key mechanism underlying the GS phenotype. From the lipidomic analysis, key observations include a reduction in triacylglycerols and elevated amounts of cardiolipins, a characteristic lipid class associated with oxidative stress, in GS phenotype. Conclusion While the triggers to the activation of endoplasmic reticulum stress are still unknown, data from this study point towards a nutritional deficiency as an underlying driver of this phenotype.

Excessive level of dietary insect protein negatively changed growth metabolomic and transcriptomic profiles of largemouth bass (Micropterus salmoides)

“…The increase in proteins and transcripts involved in protein processing in the ER and proteolysis has been previously reported in less feed efficient chinook salmon ( Esmaeili et al., 2021 ). Endoplasmic reticulum stress was postulated to be triggered by a nutritional deficiency and was regarded as a key mechanism in the stunted growth of seawater rainbow trout ( Morro et al., 2021 ). It was previously reported that feeding juvenile largemouth bass with a high carbohydrate diet also induced ER stress and oxidative stress in the intestine ( Zhao et al., 2021 ).…”

Full-Length Transcriptomes and Sex-Based Differentially Expressed Genes in the Brain and Ganglia of Giant River Prawn Macrobrachium rosenbergii

“…ERGIC-53, which was used as an ER export determinant, was found to be highly expressed only in the male nerve ganglion of giant freshwater prawn, suggesting that it facilitates the secretion of protein, including neuropeptides and hormones that are transported to the Golgi for delivery to their final destinations. Rainbow trout that are transferred from freshwater to seawater experience growth stunting and down-regulation in growth factor IGF-I transcription, revealing endoplasmic reticulum stress to be a key mechanism underlying this growth stunting phenotype [ 48 ]. The maintenance of intracellular hormones can be controlled by correctly folded models, and misfolded proteins in the endoplasmic reticulum are eliminated by a highly effective protein degradation process known as ERAD.…”

Gilthead Seabream Liver Integrative Proteomics and Metabolomics Analysis Reveals Regulation by Different Prosurvival Pathways in the Metabolic Adaptation to Stress

“…The upregulation of different aminoacyl-tRNA synthetases and several translation-related proteins ( Table S3 ) corroborated this hypothesis. Furthermore, previous studies have reported an upregulation of ER stress in seawater-transferred rainbow trout livers [ 36 ], common carp exposed to hydrogen peroxide [ 37 ], rainbow trout following overcrowding stress [ 38 ], and gilthead seabream exposed to low temperatures [ 39 ]. On the other hand, PDIP5 was found to be downregulated in hypoxia-exposed fish, exposing again the divergent responses of NET and HYP fish according to the challenge severity.…”