Effects of Increased CO2 on Fish Gill and Plasma Proteome

Abstract

Ocean acidification and warming are both primarily caused by increased levels of atmospheric CO2, and marine organisms are exposed to these two stressors simultaneously. Although the effects of temperature on fish have been investigated over the last century, the long-term effects of moderate CO2 exposure and the combination of both stressors are almost entirely unknown. A proteomics approach was used to assess the adverse physiological and biochemical changes that may occur from the exposure to these two environmental stressors. We analysed gills and blood plasma of Atlantic halibut (Hippoglossus hippoglossus) exposed to temperatures of 12°C (control) and 18°C (impaired growth) in combination with control (400 µatm) or high-CO2 water (1000 µatm) for 14 weeks. The proteomic analysis was performed using two-dimensional gel electrophoresis (2DE) followed by Nanoflow LC-MS/MS using a LTQ-Orbitrap. The high-CO2 treatment induced the up-regulation of immune system-related proteins, as indicated by the up-regulation of the plasma proteins complement component C3 and fibrinogen β chain precursor in both temperature treatments. Changes in gill proteome in the high-CO2 (18°C) group were mostly related to increased energy metabolism proteins (ATP synthase, malate dehydrogenase, malate dehydrogenase thermostable, and fructose-1,6-bisphosphate aldolase), possibly coupled to a higher energy demand. Gills from fish exposed to high-CO2 at both temperature treatments showed changes in proteins associated with increased cellular turnover and apoptosis signalling (annexin 5, eukaryotic translation elongation factor 1γ, receptor for protein kinase C, and putative ribosomal protein S27). This study indicates that moderate CO2-driven acidification, alone and combined with high temperature, can elicit biochemical changes that may affect fish health.

Effects of Water Acidification on Senegalese Sole Solea senegalensis Health Status and Metabolic Rate: Implications for Immune Responses and Energy Use

“…In fact, juvenile spotted wolfish (Anarhichas minor Olafsen) showed reduced growth and plasma chloride levels after 10 weeks exposure to pH 6.45 (Foss et al, 2003) while Atlantic salmon post-smolt (Salmo salar) growth decreased linearly with the increase of water CO 2 (Mota et al, 2019). Moreover, Bresolin de Souza et al (2014) observed an up-regulated expression of plasma immune system-and gill metabolism-related proteins in response to high CO 2 . In addition, Wang et al (2010) showed that elevated CO 2 inhibits LPS-induced expression of IL6 and TNF and impairs bacterial clearance through inhibition of both phagocytosis and autophagy in macrophages.…”

“…In fact, in salmonids production the concentration of CO 2 can reach 10-20 mg L −1 (Mota et al, 2019), while the guidelines for intensive RAS production has proposed a safe limit of 40 mg L −1 CO 2 (Blancheton, 2000;Ellis et al, 2017). Moreover, as a known consequence of anthropogenic activity, the release of CO 2 into the atmosphere is absorbed by the oceans leading to the decrease of oceanic water pH (Bresolin de Souza et al, 2014). In both scenarios, and despite the great despair in pH values found in aquaculture and in oceans (Ellis et al, 2017), the increase of water CO 2 leads to higher physiological pCO 2 in the fish.…”

“…In addition, Wang et al (2010) showed that elevated CO 2 inhibits LPS-induced expression of IL6 and TNF and impairs bacterial clearance through inhibition of both phagocytosis and autophagy in macrophages. Atlantic halibut (Hippoglossus hippoglossus) exposed to high CO 2 showed upregulation of plasma immune-related proteins as the complement component C3 and gills metabolism-and cellular turnoverrelated proteins, possibly due to an increase of energy demand (Bresolin de Souza et al, 2014). Hence, the fish immune system could also be affected acutely by hypercapnia since immune cells internal milieu is directly affected and reflects the external environment (Boleza et al, 2001).…”

Climate change and aquaculture: considering biological response and resources

“…In Atlantic halibut Hippoglossus hippoglossus, different temperatures can result in differences in down-or up-regulation of immune system-related proteins under elevated CO 2 (Bresolin de Souza et al 2014), whereas increased temperature has been as sociated with increased aerobic scope and cardiac performance, but more so under elevated CO 2 (Gräns et al 2014). For the anemonefish Amphi prion melanopus, elevated temperature had a much stronger influence on reproductive traits compared to a minimal influence of elevated CO 2 , but offspring quality declined under both increased temperature and CO 2 .…”

Characterization of a γ-aminobutyrate type A receptor-associated protein gene, which is involved in the response of Portunus trituberculatus to CO2 -induced ocean acidification

“…Ocean acidification has highly variable effects on marine organisms and marine ecosystems (Doney, Fabry, Feely, & Kleypas, ). Ocean acidification had some effects on survival (Christopher, Swiney, & Foy, ), metabolism (Pimentel et al., ), immunity (Bresolin de Souza, Jutfelt, Kling, Förlin, & Sturve, ), biological calcification (Chan et al., ; Courtney, Westfield, & Ries, ), growth and development of many marine organisms (Allan, Miller, McCormick, Domenici, & Munday, ; Bignami, Sponaugle, & Cowen, ; Forsgren, Dupont, Jutfelt, & Amundsen, ; Munday, Donelson, Dixson, & Endo, ; Munday, Dixson, et al., ; Rossi et al., ). Besides, OA did impair sensory systems and behaviours of marine vertebrates and invertebrates.…”