The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia

Abstract

Background Increases in ocean temperatures and in the frequency and severity of hypoxic events are expected with climate change, and may become a challenge for cultured Atlantic salmon and negatively affect their growth, immunology and welfare. Thus, we examined how an incremental temperature increase alone (Warm & Normoxic-WN: 12 → 20 °C; 1 °C week− 1), and in combination with moderate hypoxia (Warm & Hypoxic-WH: ~ 70% air saturation), impacted the salmon’s hepatic transcriptome expr\ession compared to control fish (CT: 12 °C, normoxic) using 44 K microarrays and qPCR. Results Overall, we identified 2894 differentially expressed probes (DEPs, FDR < 5%), that included 1111 shared DEPs, while 789 and 994 DEPs were specific to WN and WH fish, respectively. Pathway analysis indicated that the cellular mechanisms affected by the two experimental conditions were quite similar, with up-regulated genes functionally associated with the heat shock response, ER-stress, apoptosis and immune defence, while genes connected with general metabolic processes, proteolysis and oxidation-reduction were largely suppressed. The qPCR assessment of 41 microarray-identified genes validated that the heat shock response (hsp90aa1, serpinh1), apoptosis (casp8, jund, jak2) and immune responses (apod, c1ql2, epx) were up-regulated in WN and WH fish, while oxidative stress and hypoxia sensitive genes were down-regulated (cirbp, cyp1a1, egln2, gstt1, hif1α, prdx6, rraga, ucp2). However, the additional challenge of hypoxia resulted in more pronounced effects on heat shock and immune-related processes, including a stronger influence on the expression of 14 immune-related genes. Finally, robust correlations between the transcription of 19 genes and several phenotypic traits in WH fish suggest that changes in gene expression were related to impaired physiological and growth performance. Conclusion Increasing temperature to 20 °C alone, and in combination with hypoxia, resulted in the differential expression of genes involved in similar pathways in Atlantic salmon. However, the expression responses of heat shock and immune-relevant genes in fish exposed to 20 °C and hypoxia were more affected, and strongly related to phenotypic characteristics (e.g., growth). This study provides valuable information on how these two environmental challenges affect the expression of stress-, metabolic- and immune-related genes and pathways, and identifies potential biomarker genes for improving our understanding of fish health and welfare.

Atlantic Salmon (Salmo salar) Cage-Site Distribution, Behavior, and Physiology During a Newfoundland Heat Wave

“…Our data, in combination with other recently published data (Gamperl et al, 2020 ; Zanuzzo et al, 2020 ; Beemelmanns et al, 2021a , b , c ; and see references above), also provide vital/key new information on how conditions at salmon cage-sites during the summer/early fall are likely to impact these fish in Atlantic Canada and suggest that a multi-faceted approach may/will be needed to prevent potential losses at salmon cage-sites under current climate change scenarios (see IPCC, 2019 ). Given recent data which suggest that Atlantic salmon of Saint John River stock can survive long-term exposure to temperatures of > 21°C in combination with moderate hypoxia (60–70% air saturation) and that unlike fish in Tasmania (Stehfest et al, 2017 ; Wade et al, 2019 ) have not yet experienced these temperatures, it is clear that selective breeding for upper thermal tolerance (given its effects on food consumption, growth, and stress biomarkers; Gamperl et al, 2020 ; Beemelmanns et al, 2021a , b ) is not only needed to improve production in the summer and to prevent losses that are predicted to get worse given rising average ocean temperatures and more frequent/severe heat waves. Better vaccines against bacterial and viral diseases and mitigating strategies/treatments for pathogen outbreaks (incl.…”

“…A report commissioned to determine the cause of the mortalities (Burke et al, 2020 ) concluded that these environmental conditions were the primary cause of the large number of salmon deaths. However, more recent data on the effects of these conditions on fish physiology (Gamperl et al, 2020 , Zanuzzo et al, 2020 ; Beemelmanns et al, 2021a , b , c ), and contained in this study, do not support this assertion. For example, the salmon in the cage in which we had fish did not experience temperatures > 19.5°C; large (> 800 g) salmon from similar stocks have been shown to tolerate elevated temperatures as high as 21°C for prolonged periods when combined with water O 2 levels of 60–70% saturation (lower than the lowest O 2 levels reported in the cages) without mortalities (Gamperl et al, 2020 ); salmon from Norway and Tasmania can tolerate prolonged exposure to similar temperatures (Hvas et al, 2017 ; Tromp et al, 2018 ); the critical oxygen tension/limiting oxygen saturation (LOS) for Atlantic salmon is ~63–67% at 22°C (Barnes et al, 2011 ; Remen et al, 2013 ), well below the water oxygen level reported in the cages by Burke et al ( 2020 ); and all the salmon implanted with data loggers that survived for several weeks post-implantation experienced similar conditions to those reported in the summer of 2019.…”

PacBio Isoform Sequencing and Illumina RNA Sequencing Provide Novel Insights on Responses to Acute Heat Stress in Apostichopus japonicus Coelomocytes

“…Our results suggest a potential role of HSPs in the immune system of sea cucumber coelomocytes under HS. Similar results have also been reported in some fish species such as rainbow trout Oncorhynchus mykiss (Huang et al, 2018) and Atlantic salmon Salmo salar (Beemelmanns et al, 2021).…”

Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa

“…In Oncorhynchus kisutch, hypoxia generated a cortisol stress response ≤35% DO levels and several toll-like receptors and cytokines of the innate and adaptive immune response were differentially regulated (Martínez et al, 2020). Transcriptome analyses revealed combined effects of hypoxia and high water temperature (20 • C) on hepatic expression of immune and stress genes in Atlantic salmon (Beemelmanns et al, 2021).…”