Histological and transcriptomic analysis of muscular atrophy associated with depleted flesh pigmentation in Atlantic salmon (Salmo salar) exposed to elevated seawater temperatures

Abstract

Tasmania is experiencing increasing seawater temperatures during the summer period which often leads to thermal stress-induced starvation events in farmed Atlantic salmon, with consequent flesh pigment depletion. Our previous transcriptomic studies found a link between flesh pigmentation and the expression of genes regulating lipid metabolism accompanied by feeding behavior in the hindgut. However, the impact of prolonged exposure to elevated water temperature on muscle structural integrity and molecular mechanisms in muscle underlying pigment variation has not been elucidated to date. In this study, we investigated the effect of prolonged exposure to elevated water temperature on the farmed salmon flesh pigmentation and structural integrity, using muscle histological and transcriptomic analysis. On April 2019, after the end of the summer, two muscle regions of the fish fillet, front dorsal and back central (usually the most and least affected by depletion, respectively), were sampled from fifteen fish (weighing approximately 2 kg and belonging to the same commercial population split in two cages). The fish represented three flesh color intensity groups (n = 5 fish per group) categorized according to general level of pigmentation and presence of banding (i.e. difference in color between the two regions of interest) as follows: high red color-no banding (HN), high red color-banded (HB) and Pale fish. Histological analysis showed a distinction between the flesh color intensity phenotypes in both muscle regions. Muscle fibers in the HB fish were partly degraded, while they were atrophied and smaller in size in Pale fish compared to HN fish. In the Pale fish, interstitial spaces between muscle fibers were also enlarged. Transcriptomic analysis showed that in the front dorsal region of the HN fish, genes encoding collagens, calcium ion binding and metabolic processes were upregulated while genes related to lipid and fatty acid metabolism were downregulated when compared to HB fish. When comparing the back central region of the three phenotypes, actin alpha skeletal muscle and myosin genes were upregulated in the HN and HB fish, while tropomyosin genes were upregulated in the Pale fish. Also, genes encoding heat shock proteins were upregulated in the HN fish, while genes involving lipid metabolism and proteolysis were upregulated in the Pale fish. Starvation, likely caused by thermal stress during prolonged periods of elevated summer water temperatures, negatively affects energy metabolism to different extents, leading to localized or almost complete flesh color depletion in farmed Atlantic salmon. Based on our results, we conclude that thermal stress is responsible not only for flesh discoloration but also for loss of muscle integrity, which likely plays a key role in pigment depletion.

High-Temperature Stress Induces Autophagy in Rainbow Trout Skeletal Muscle

“…Similarly, in the African sharptooth catfish (Clarias gariepinus), it was reported that the long-term exposure to hightemperature stress has a negative consequence on skeletal muscle growth performance and structural integrity [31]. In Atlantic salmon (Salmo salar), thermal stress has been shown to cause skeletal muscle discoloration and loss of skeletal muscle integrity [32], while in gilt-head seabream (Sparus aurata), exposure to high temperatures induces an inflammatory and oxidative response in red muscle [33]. To gain further insights into the molecular mechanisms underlying these responses, we conducted RNA-Seq analysis in the present study.…”

A warming western boundary current increases the prevalence of commercially disruptive parasites in broadbill swordfish

“…In addition to changing pathogen and disease dynamics, climate‐driven environmental change can affect the nutritional and sensory quality of commercially important seafood species (Shalders et al, 2022). For example, higher water temperatures and warm climate modes—such as El Niño—can exacerbate the prevalence of non‐pathogen meat‐quality issues in high‐value fish, such as chalky halibut syndrome (Kaimmer, 2000), burnt tuna (Watson, 1995), burnt amberjack (Mora et al, 2007), flesh discoloration and muscular atrophy in Atlantic salmon (Vo et al, 2023) and potentially mushy tuna syndrome (Bakun & Broad, 2001), which can increase loss and wastage for seafood companies. This creates a problem for countries seeking to meet international waste targets as part of the United Nations Sustainable Development Goals (United Nations, 2015), and it presents issues for not only food and nutrition security in small‐scale fisheries (Thilsted et al, 2016) but also profitability and sustainability in high‐value, export‐driven fisheries (Bolin, Schoeman, et al, 2021).…”