Atlantic salmon represent a major component of the aquaculture industry with an annual production value of 16.7 billion USD in 2017, the largest for any finfish and the second highest of all marine species (Houston et al, 2020). This industry suffers from a high mortality rate. In Scottish aquaculture, salmon production losses remained stable at around 20% between 1990 and 2014 (Murray and Munro, 2018). However, this has increased in recent years with the latest smolt input to harvest loss rate standing at 25.6% (Munro, 2022). High mortality in farmed salmon production is not specific to UK aquaculture with approximately 20% of Norwegian farmed salmon also failing to reach the end of the production line (Directorate of Fisheries, 2019).
This is the result of low robustness, with viral diseases including cardiomyopathy syndrome and pancreas disease, bacterial diseases including tenacibaculosis, and parasites (especially salmon lice) accounting for much of this loss during the seawater production phase. The increased mortality among salmon is indicative of impaired immunity.
The environmental and production factors contributing to this effect are not properly understood. One potential cause of low robustness and impaired immunity may be attributed to suboptimal temperature during embryogenesis. As poikilothermic organisms, temperature influences essentially all biochemical and physiological processes of fishes like Atlantic salmon. It has been shown in many organisms including Atlantic salmon, that exposure to external stimuli such as temperature during early development may permanently alter metabolism and physiology, even long after the stimuli has been removed (Ziqiang et al., 2019). This phenomenon is known as metabolic programming. Higher embryonic temperature has been shown to accelerate growth of Atlantic salmon (Austreng et al, 1987) resulting in larger sized muscle fibres containing significantly more myofibrillar material. Muscle cell size increase was also found to proceed at a greater pace in higher embryonic temperature groups relative to lower temperature groups (Stickland et al, 1988). Additionally, higher embryonic temperature was linked to decreased promotor methylation in the Atlantic salmon myogenin gene, a transcription factor essential for muscle tissue development, which was in turn correlated with increased myogenin expression (Burgerhout et al, 2017).
However, growth of embryos at higher temperatures has been shown to result in greater rates of mortality and abnormal development (Gunnes, 1978). It is possible that metabolic programming of an embryo towards fast growth may impair energetic allocation into other functions and processes. For example, in coho salmon, fast-growing transgenic fish overexpressing growth hormone showed evidence of decreased immune function compared with wild-type fish (Alzaid et al, 2018). This suggests a fine balance is normally maintained between various physiological systems, which may become disrupted when the organism is pushed too strongly towards growth.
The COOLFISH project, in which my PhD is embedded, seeks to fully understand the effects of such metabolic programming by early rearing temperature on Atlantic salmon development and health throughout the production cycle. Three groups of Atlantic salmon were grown under different temperatures (4, 6 and 8°C) during embryogenesis (solely from fertilization to the eyed stage). After the embryos reached the eyed stage, these groups were reared under a common temperature for the rest of their life (until the parr stage, when a final disease challenge was performed using Yersinia ruckeri). Fish were sampled at start feeding, early in development and after the immune challenge.
My PhD aims to understand the functional mechanisms driving temperature differences in immune function, taking a multi-omics approach. At the conference single nucleus sequencing data of livers taken at start feeding sampling will be presented. Analysis is currently at an early stage but will be completed before September. Preliminary results show hundreds of differentially expressed genes found in hepatocytes and immune cell clusters between the temperature groups. This will be paired with freshly generated proteomics data (n=9 per temp group) from matched samples confirming the link between transcription levels and the actual abundance of proteins, strengthening the link between the cell-specific transcriptome and phenotype.