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- Increased intestinal carbonate precipitate abundance in the sea bream (Sparus aurata L.) in response to ocean acidificationPublication . Gregorio, Silvia; Ruiz-Jarabo, Ignacio; Carvalho, Edison S. M.; Fuentes, JuanMarine fish contribute to the carbon cycle by producing mineralized intestinal precipitates generated as by-products of their osmoregulation. Here we aimed at characterizing the control of epithelial bicarbonate secretion and intestinal precipitate presence in the gilthead sea bream in response to predicted near future increases of environmental CO2. Our results demonstrate that hypercapnia (950 and 1800 μatm CO2) elicits higher intestine epithelial HCO3- secretion ex vivo and a subsequent parallel increase of intestinal precipitate presence in vivo when compared to present values (440 μatm CO2). Intestinal gene expression analysis in response to environmental hypercapnia revealed the up-regulation of transporters involved in the intestinal bicarbonate secretion cascade such as the basolateral sodium bicarbonate co-transporter slc4a4, and the apical anion transporters slc26a3 and slc26a6 of sea bream. In addition, other genes involved in intestinal ion uptake linked to water absorption such as the apical nkcc2 and aquaporin 1b expression, indicating that hypercapnia influences different levels of intestinal physiology. Taken together the current results are consistent with an intestinal physiological response leading to higher bicarbonate secretion in the intestine of the sea bream paralleled by increased luminal carbonate precipitate abundance and the main related transporters in response to ocean acidification.
- Changes in plasma amino acid levels in a euryhaline fish exposed to different environmental salinitiesPublication . Aragão, C.; Costas, B.; Vargas-Chacoff, L.; Ruiz-Jarabo, I.; Dinis, Maria Teresa; Mancera, J. M.; Conceição, L. E. C.Previous studies have shown that Senegalese sole is partially euryhaline in the juvenile phase, being able to adapt to a wide range of salinities in a short-time period, due to changes at the osmoregulatory and metabolic level. This study aimed to assess the effects of acclimation of sole to a wide range of salinities, with a special emphasis on the role of plasma amino acids during this process. Sole juveniles were acclimated for 2 weeks to different salinities: 5, 15, 25, 38, and 55 g L−1. Plasma levels of cortisol, glucose, osmolality, and free amino acids were assessed at the end. Changes in plasma levels of cortisol, glucose, and amino acids indicate that fish reared at 5 and 55 g L−1 were facing extra energy costs. Amino acids seem to play an important role during salinity acclimation, either as energy sources or as important osmolytes for cell volume regulation.
- Intestinal response to ocean acidification in the European sea bass (Dicentrarchus labrax)Publication . Alves, Alexandra; Gregorio, Silvia F.; Ruiz-Jarabo, Ignacio; Fuentes, Juanthe intestine of marine fishes contributes to the ocean carbon cycle producing carbonate aggregates as part of the osmoregulatory process. Therefore, this study aimed to evaluate physiological adjustments of European sea bass (Dicentrarchus labrax) intestine to a higher pCO(2) environment likely in the near future (similar to 1700 mu atm). At the whole-body level, hypercapnia for 5 weeks resulted in fish having a significantly diminished specific growth rate, condition factor and hepatosomatic index. An increase in plasma osmolality and HCO3- concentration was detected, paralleled by decreased metabolites concentrations. In the intestine, high seawater pCO(2) was without effect on ouabain-sensitive ATPase activities, while Bafilomycin A1-sensitive ATPase activity significantly decreased in the anterior intestine. Anterior and mid intestine were mounted in Ussing chambers in order to measure bioelectrical parameters and bicarbonate secretion by pH-Stat ex-vivo. Hypercapnia induced a 2.3 and 2.8-fold increase in bicarbonate secretion rates in the anterior and mid intestine, respectively. In the intestinal fluid, HCO3- concentration increased 2.2-fold, and carbonate precipitates showed a 4.4-fold increase in response to hypercapnia, paralleled by a > 3-fold increase of drinking and a > 2-fold increase of intestinal volume at any given time. At the molecular level, hypercapnia elicited higher intestinal mRNA expression levels for atp6v1b (V-ATPase B subunit), slc4a4, slc26a3, and slc26a6, both in the anterior and mid intestine. As a whole, our results show that the intestine of sea bass responds to high seawater pCO(2), a response that comes at a cost at the whole-body level with an impact in the fish specific growth rate, condition factor, and hepatosomatic index.
- Intestinal response to salinity challenge in the Senegalese sole (Solea senegalensis)Publication . Ruiz-Jarabo, I.; Barany, A.; Jerez-Cepa, I.; Mancera, J. M.; Fuentes, JuanFish are continuously forced to actively absorb or expel water and ions through epithelia. Most studies have focused on the gill due to its role in Na+ and Cl- trafficking. However, comparatively few studies have focused on the changing function of the intestine in response to external salinity. Therefore, the present study investigated the main intestinal changes of long-term acclimation of the Senegalese sole (Solea senegalensis) to 5,15, 38 and 55 ppt. Through the measurement of short-circuit current (Isc) in Ussing chambers and biochemical approaches, we described a clear anterior/posterior functional regionalization of the intestine in response to salinity. The use of specific inhibitors in Ussing chamber experiments, revealed that the bumetanide-sensitive Na+/K+/Cl- co-transporters are the main effectors of Cl- uptake in both anterior intestine and rectum. Additionally, the use of the anion exchanger specific inhibitor, DIDS, showed a salinity/region dependency of anion exchanger function. Moreover, we also described ouabain-sensitive Na+/K+-ATPase (NKA) and Bafilomycin Al-sensitive H-ATPase activities (HA), which displayed changes related to salinity and intestinal region. However, the most striking result of the present study is the description of an omeprazole-sensitive H+/K+-ATPase (HKA) in the rectum of Senegalese sole. Its activity was consistently measurable and increased at lower salinities, reaching rates even higher than those of the NKA. Together our results provide new insights into the changing role of the intestine in response to external salinity in teleost fish. The rectal activity of HKA offers an alternative/cooperative mechanism with the HA in the final processing of intestinal water absorption by apical titration of secreted bicarbonate. (C) 2016 Elsevier Inc. All rights reserved.
- Different environmental temperatures affect amino acid metabolism in the eurytherm teleost Senegalese sole (Solea senegalensis Kaup, 1858) as indicated by changes in plasma metabolitesPublication . Costas, B.; Aragão, C.; Ruiz-Jarabo, I.; Vargas-Chacoff, L.; Arjona, F. J.; Mancera, J. M.; Dinis, Maria Teresa; Conceição, L. E. C.Senegalese sole (Solea senegalensis) is a eurytherm teleost that under natural conditions can be exposed to annual water temperature fluctuations between 12 and 26C. This study assessed the effects of temperature on sole metabolic status, in particular in what concerns plasma free amino acid changes during thermal acclimation.
- Survival rates and physiological recovery responses in the lesser-spotted catshark (Scyliorhinus canicula) after bottom-trawlingPublication . Barragan-Mendez, C.; Ruiz-Jarabo, I.; Fuentes, Juan; Mancera, J. M.; Sobrino, I.In 2019, Europe will adopt a no-discards policy in fisheries. This entails the landing of captured species unless strong evidence is provided supporting their survival and recovery after fishing. Thus, research on this topic is gaining momentum. Bottom-trawling, as a non-selective fishing method, is characterized by a high proportion of discards including vulnerable key species, such as demersal sharks. Their survival may also depend on capture depth. By paralleling onboard and laboratory experiments with the small-spotted catshark, Scyliorhinus canicula, we offer a robust experimental design to assess the survival of discarded sharks. Catsharks were captured by bottom-trawling at two depths (shallow similar to 89 m and deep similar to 479 m). Blood samples were collected following trawl capture and analyzed for stress biomarkers (lactate, osmolality, phosphate, urea). During recovery in onboard tanks, behavior was video-recorded and fish were re-sampled after 24 h. A second experiment was conducted in laboratory facilities to simulate air-exposure after trawling and to analyze the physiological recovery. Our results showed that 95.7% of the animals survived 24 h after trawling. We confirmed that trawling elicited acute stress responses in catshark but that they managed to recover. This was demonstrated by lactate concentrations that were 2.6 mM upon capture, but recovered to assumed baselines after 24 h (0.2 mM). Non-invasive video monitoring revealed behavioral differences with depth, whereby those captured at 89 m depth required longer to recover than those captured at 479 m depth. Implementation of standardized survival studies by fishery managers can benefit from holistic physiological approaches, such as the one proposed here.
- Physiological short-term response to sudden salinity change in the Senegalese sole (Solea senegalensis)Publication . Herrera, M.; Aragão, C.; Hachero-Cruzado, Ismael; Ruiz-Jarabo, I.; Vargas-Chacoff, L.; Mancera, J. M.; Conceição, L. E. C.The physiological responses of Senegalese sole to a sudden salinity change were investigated. The fish were first acclimated to an initial salinity of 37.5 ppt for 4 h. Then, one group was subjected to increased salinity (55 ppt) while another group was subjected to decreased salinity (5 ppt). The third group (control group) remained at 37.5 ppt. We measured the oxygen consumption rate, osmoregulatory (plasma osmolality, gill and kidney Na+,K+-ATPase activities) and stress (plasma cortisol and metabolites) parameters 0.5 and 3 h after transfer. Oxygen consumption at both salinities was higher than for the control at both sampling times. Gill Na+,K+-ATPase activity was significantly higher for the 55 ppt salinity at 0.5 h. Plasma osmolality decreased in the fish exposed to 5 ppt at the two sampling times but no changes were detected for high salinities. Plasma cortisol levels significantly increased at both salinities, although these values declined in the low-salinity group 3 h after transfer. Plasma glucose at 5 ppt salinity did not vary significantly at 0.5 h but decreased at 3 h, while lactate increased for both treatments at the first sampling time and returned to the control levels at 3 h. Overall, the physiological response of S. senegalensis was immediate and involved a rise in oxygen consumption and plasma cortisol values as well as greater metabolite mobilization at both salinities.
- Physiological responses of Senegalese sole (Solea senegalensis Kaup, 1858) after stress challenge: Effects on non-specific immune parameters, plasma free amino acids and energy metabolismPublication . Costas, B.; Conceição, L. E. C.; Aragão, C.; Martos-Sitcha, J. A.; Ruiz-Jarabo, I.; Mancera, J. M.; Afonso, A.Physiological responses after an acute handling stress and their subsequent effects on innate immune parameters, plasma free amino acids (AA) and liver energy substrates were assessed in Senegalese sole (Solea senegalensis). Eight groups of six specimens (136.1± 58.4 g wet weight) were maintained undisturbed, while other eight groups of six specimens were used for acute stress challenge (air exposed during 3 min). A group of six specimens was sampled for blood and head-kidney collection immediately after air exposure (time 0), while the remaining groups were sampled at 5 and 30 min, 1, 2, 4, 6 and 24 h. Undisturbed fish were sampled at the same times and used as control. Fish were fasted for 24 h prior to air exposure and sampling. Plasma cortisol, glucose, lactate and osmolality levels increased immediately after stress peaking at 1 h in air exposed fish. Changes in plasma free AA were also observed at 1 and 24 h after stress. In liver, glycogen levels significantly decreased at 30 min and 1 h, while triglycerides values significantly increased at 1, 2 and 4 h in air exposedfish. In addition, total AA levels in liver augmented significantly at 2 h holding high until 24 h in air exposed specimens. The respiratory burst of head-kidney leucocytes from air exposed fish was significantly higher than that from control groups at 2 and 6 h after air exposure. On the other hand, plasma lysozyme activity significantly decreased at 4 h after acute stress in air exposed fish, while plasma alternative complement pathway followed an inverse linear relationship with respect to cortisol showing the lowest value at 1 h after air exposure. The present study suggests that Senegalese sole presents a stress response comparable to that observed in other teleosts. While some indispensable AA may be used for the synthesis of compounds related to the stress response or fatty acid transport, dispensable AA were probably mainly employed either as energy sources or in gluconeogenesis. Moreover, results from non-specific immune parameters assessed suggest that cortisol may act as regulator of the innate immune system.
- Metabolic responses to salinity changes in the subantarctic notothenioid teleost Eleginops maclovinusPublication . Vargas-Chacoff, L.; Moneva, F.; Oyarzun, R.; Martinez, D.; Saavedra, E.; Ruiz-Jarabo, I.; Munoz, J. L. P.; Bertran, C.; Mancera, J. M.Eleginops maclovinus is an endemic, subantarctic Notothenioidei species. This study examined the influence of different environmental salinities (5, 15, and 45 psu; and 32 psu as a control) on energy metabolism in E. maclovinus over a period of 14 days. Metabolite contents and enzymatic activities related to carbohydrate, amino acid, and lipid metabolisms were evaluated in metabolic (liver) and osmoregulatory (gill and kidney) tissues. At extreme salinities (5 and 45 psu), the liver showed a high consumption of energy reserves, mainly as amino acids and carbohydrates. Carbohydrate metabolism in the gills did not change under different salinities, but increased lactate levels were found, suggesting that this tissue may use lactate as an energy substrate. Amino acid metabolism in the gills decreased at 5 psu but increased at 45 psu, and lipid metabolism increased at 5 and 15 psu during the first days of the trial, indicating a possible use of lipids as energy. Kidney carbohydrate catabolism and amino acid metabolism increased after 14 days at 45 psu, while lipid metabolism did not vary in relation to salinity changes. Together, these results suggest that the liver is most affected by salinity changes, probably due to its role as a supplier of energetic substrates. The gills and kidney, osmoregulatory tissues, maintained their energy metabolism levels with minor modifications. In conclusion, E. maclovinus exhibits metabolic adjustments to adapt to different salinities, showing the best responses in isosmotic environmental salinities.
- Ocean acidification compromises energy management in Sparus aurata (Pisces: Teleostei)Publication . Ruiz-Jarabo, I.; Gregorio, SF; Alves, Alexandra; Mancera, J. M.; Fuentes, JuanThe effects of ocean acidification mediated by an increase in water pCO(2) levels on marine organisms are currently under debate. Elevated CO2 concentrations in the seawater induce several physiological responses in teleost fish, including acid-base imbalances and osmoregulatory changes. However, the consequences of CO2 levels enhancement on energy metabolism are mostly unknown. Here we show that 5 weeks of exposure to hypercapnia (950 and 1800 mu atm CO2) altered intermediary metabolism of gilthead seabream (Sparus aurata) compared to fish acclimated to current ocean values (440 mu atm CO2). We found that seabream compromises its physiological acid-base balance with increasing water CO2 levels and the subsequent acidification. Intestinal regions (anterior, mid, and rectum) engaged in maintaining this balance are thus altered, as seen for Na+/K+ ATPase and the vacuolar-type H+-ATPase activities. Moreover, liver and muscle counteracted these effects by increasing catabolic routes e.g., glycogenolysis, glycolysis, amino acid turnover, and lipid catabolism, and plasma energy metabolites were altered. Our results demonstrate how a relatively short period of 5 weeks of water hypercapnia is likely to disrupt the acid-base balance, osmoregulatory capacity and intermediary metabolism in S. aurata. However, long-term studies are necessary to fully understand the consequences of ocean acidification on growth and other energy-demanding activities, such as reproduction.