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Early Developmental Stress Affects Subsequent Gene Expression Response to an Acute Stress in Atlantic Salmon: An Approach for Creating Robust Fish for Aquaculture?

ABSTRACT: Stress during early life has potential to program and alter the response to stressful events and metabolism in later life. Repeated short exposure of Atlantic salmon to cold water and air during embryonic (E), post-hatch (PH) or both phases of development (EPH) has been shown to alter the methylome and transcriptome and to affect growth performance during later life compared to untreated controls (CO). The aim of this study was to investigate how the transcriptome of these fish responds to subsequent acute stress at the start feeding stage, and to describe methylation differences that might steer these changes. EPH treated fish showed the strongest down-regulation of corticotropin releasing factor 1, up-regulation of glucocorticoid receptor and 3-oxo-5-alpha-steroid 4-dehydrogenase 2 gene expression and a suppressed cortisol response 3 hr after the acute stress, differences that could influence hormesis and be affecting how EPH fish cope and recover from the stress event. Growth hormone 2 and insulin-like growth factor 1 were more strongly down-regulated following acute stress in EPH treated fish relative to E, PH and CO fish. This indicates switching away from growth toward coping with stress following stressful events in EPH fish. Genes implicated in immune function such as major histocompatibility class 1A, T-cell receptor and toll-like receptor also responded to acute stress differently in EPH treated fish, indicating that repeated stresses during early life may affect robustness. Differential DNA methylation was detected in regions mapping <500 bases from genes differentially responding to acute stress suggesting the involvement of epigenetic mechanisms. Stress treatments applied during early development therefore have potential as a husbandry tool for boosting the productivity of aquaculture by affecting how fish respond to stresses at critical stages of production.

SUBMITTER: Robinson NA

PROVIDER: S-EPMC6505151 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Early Developmental Stress Affects Subsequent Gene Expression Response to an Acute Stress in Atlantic Salmon: An Approach for Creating Robust Fish for Aquaculture?

Robinson Nicholas A NA Johnsen Hanne H Moghadam Hooman H Andersen Øivind Ø Tveiten Helge H

G3 (Bethesda, Md.) 20190507 5

Stress during early life has potential to program and alter the response to stressful events and metabolism in later life. Repeated short exposure of Atlantic salmon to cold water and air during embryonic (E), post-hatch (PH) or both phases of development (EPH) has been shown to alter the methylome and transcriptome and to affect growth performance during later life compared to untreated controls (CO). The aim of this study was to investigate how the transcriptome of these fish responds to subse ...[more]

PMID: 30885921

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Project description:UnlabelledReliance on fishmeal as a primary protein source is among the chief economic and environmental concerns in aquaculture today. Fishmeal-based feeds often require harvest from wild fish stocks, placing pressure on natural ecosystems and causing price instability. Alternative diet formulations without the use of fishmeal provide a potential solution to this challenge. Although the impact of alternative diets on fish performance, intestinal inflammation, palatability, and gut microbiota has been a topic of recent interest, less is known about how alternative feeds impact the aquaculture environment as a whole. The recent focus on recirculating aquaculture systems (RAS) and the closed-containment approach to raising food fish highlights the need to maintain stable environmental and microbiological conditions within a farm environment. Microbial stability in RAS biofilters is particularly important, given its role in nutrient processing and water quality in these closed systems. If and how the impacts of alternative feeds on microbial communities in fish translate into changes to the biofilters are not known. We tested the influence of a fishmeal-free diet on the microbial communities in RAS water, biofilters, and salmon microbiomes using high-throughput 16S rRNA gene V6 hypervariable region amplicon sequencing. We grew Atlantic salmon (Salmo salar) to market size in six replicate RAS tanks, three with traditional fishmeal diets and three with alternative-protein, fishmeal-free diets. We sampled intestines and gills from market-ready adult fish, water, and biofilter medium in each corresponding RAS unit. Our results provide data on how fish diet influences the RAS environment and corroborate previous findings that diet has a clear influence on the microbiome structure of the salmon intestine, particularly within the order Lactobacillales (lactic acid bacteria). We conclude that the strong stability of taxa likely involved in water quality processing regardless of diet (e.g., Nitrospira) may further alleviate concerns regarding the use of alternative feeds in RAS operations.ImportanceThe growth of the aquaculture industry has outpaced terrestrial livestock production and wild-capture fisheries for over 2 decades, currently producing nearly 50% of all seafood consumed globally. As wild-capture fisheries continue to decline, aquaculture's role in food production will grow, and it will produce an estimated 62% of all seafood consumed in 2020. A significant environmental concern of the industry is the reliance on fishmeal as a primary feed ingredient, as its production still requires harvest from wild fisheries. Our study adds to the growing body of literature on the feasibility of alternative, fishmeal-free diets. Specifically, we asked how fishmeal-free diets influence microbial communities in recirculating salmon farms. Unlike previous studies, we extended our investigation beyond the microbiome of the fish itself and asked how alterative diets influence microbial communities in water and critical biofilter habitats. We found no evidence for adverse effects of alternative diets on any microbial habitat within the farm.

Dataset Information

Early Developmental Stress Affects Subsequent Gene Expression Response to an Acute Stress in Atlantic Salmon: An Approach for Creating Robust Fish for Aquaculture?

Publications

Early Developmental Stress Affects Subsequent Gene Expression Response to an Acute Stress in Atlantic Salmon: An Approach for Creating Robust Fish for Aquaculture?

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