Transcriptomic profiling of Gh/Igf system reveals a prompted tissue-specific differentiation and novel hypoxia responsive genes in gilthead sea bream

Abstract

A customized PCR-array was used for the simultaneous gene expression of the Gh/Igf system and related markers of muscle growth, and lipid and energy metabolism during early life stages of gilthead sea bream (60–127 days posthatching). Also, transcriptional reprogramming by mild hypoxia was assessed in fingerling fish with different history trajectories on O2 availability during the same time window. In normoxic fish, the expression of almost all the genes in the array varied over time with a prompted liver and muscle tissue-specific differentiation, which also revealed temporal changes in the relative expression of markers of the full gilthead sea bream repertoire of Gh receptors, Igfs and Igf-binding proteins. Results supported a different contribution through development of ghr and igf subtypes on the type of action of GH via systemic or direct effects at the local tissue level. This was extensive to Igfbp1/2/4 and Igfbp3/5/6 clades that clearly evolved through development as hepatic and muscle Igfbp subtypes, respectively. This trade-off is however very plastic to cope changes in the environment, and ghr1 and igfbp1/3/4/5 emerged as hypoxic imprinting genes during critical early developmental windows leading to recognize individuals with different history trajectories of oxygen availability and metabolic capabilities later in life.

Understanding how high stocking densities and concurrent limited oxygen availability drive social cohesion and adaptive features in regulatory growth, antioxidant defense and lipid metabolism in farmed gilthead sea bream (Sparus aurata)

“…At the same time, however, there are several mechanisms contributing to oxidative stress during diabetes and hyperglycemia, which is indicative that exists a delicate balance between the protective and damaging effects of glucose to maintain redox homeostasis through the evolution ( Cherkas et al, 2020 ). In the present study, the protective glucose effects in HD fish were shaped by a positive association of glucose with a number of antioxidant enzymes ( mn-sod, gpx4, prdx5 ) in the liver ( Figure 6 ) and glucose responsive proteins ( grp170, grp75 ) in skeletal muscle ( Figure 7 ), all of them already identified as highly stress-responsive genes in gilthead sea bream ( Bermejo-Nogales et al, 2008 ; Saera-Vila et al, 2009 ; Calduch-Giner et al, 2010 ; Pérez-Sánchez et al, 2013 ; Malandrakis et al, 2014 ; Magnoni et al, 2017 ; Martos-Sitcha et al, 2019a ; Naya-Català et al, 2021 ). Indeed, regardless of glucose-gene correlations, the overall trend in both liver and skeletal muscle was the upregulated expression of grp genes ( grp170, grp94 and grp75 ) in HD fish .…”

“…Of note, both behavior and swimming performance are also regulated genetically in this species ( Perera et al, 2021 ; Calduch-Giner et al, 2023 ). At the same time, swimming performance can be improved by a mild-hypoxia pre-conditioning, which leads to a persistent higher critical speed at exercise exhaustion that shifts towards a higher anaerobic fitness following normoxia restoration ( Naya-Català et al, 2021 ). It must be also taken into account that aquaculture finishing production cycle is often accounted during the summer period with relatively high stocking densities and reduced O 2 availability, and there is still a lack of practical procedures for assessing changes in behavior, physiological traits and welfare indicators in order to fulfill growth performance and welfare status with intensive aquaculture production.…”

“…It must be also taken into account that aquaculture finishing production cycle is often accounted during the summer period with relatively high stocking densities and reduced O 2 availability, and there is still a lack of practical procedures for assessing changes in behavior, physiological traits and welfare indicators in order to fulfill growth performance and welfare status with intensive aquaculture production. Thus, the present study aims to contribute to solve this gap of knowledge, combining the use of AEFishBIT data-loggers for accurate monitoring of swimming activity and breathing rates ( Calduch-Giner et al, 2022 ) with customized PCR-arrays for the simultaneous gene expression profiling of stress-responsive genes ( Calduch-Giner et al, 2010 ; Magnoni et al, 2017 ; Martos-Sitcha et al, 2019a ; Naya-Català et al, 2021 ), and welfare scores of muscle fat content, blood biochemistry, and external tissue damage ( Sánchez-Muros et al, 2013 ; Seibel et al, 2021 ; Weirup et al, 2022 ). The hypothesis of work is that such integrative approach can contribute to better determine the golden stocking density in a given farming condition, encompassing animal welfare and industry interests, with the double aim of mitigating drawback effects but also recognizing the importance of indicators of positive welfare of both physical health and appropriate social interactions ( Ashley, 2007 ; Toni et al, 2019 ).…”

Revising the Impact and Prospects of Activity and Ventilation Rate Bio-Loggers for Tracking Welfare and Fish-Environment Interactions in Salmonids and Mediterranean Farmed Fish

“…However, in gilthead sea bream juveniles, this process is more complex than initially envisaged. Thus, the resetting of the skeletal muscle transcriptome by mild hypoxia condition first primed an increased contribution of lipid metabolism to the whole energy supply to preserve the aerobic energy production, and thereafter (with the restoration of normoxia) a reduced protein turnover and improved anaerobic fitness (Naya-Català et al, 2021b). How fish physiologists, farmers and breeders can fully exploit this metabolic plasticity remains open, though it becomes clear that it can serve to preserve an efficient nutrient utilization but also the swimming performance under predictable hypoxic stress episodes.…”

Use of male-to-female sex reversal as a welfare scoring system in the protandrous farmed gilthead sea bream (Sparus aurata)

“…This includes the use of gut microbiota as a reliable criterion to evaluate the success of selective breeding for improving the performance and competitiveness of European aquaculture (5,6). At the same time, novel fish feed formulations, and epigenetic and behavioral approaches are widely applied to assure a more ethical and sustainable aquaculture production with the increase of water temperature and hypoxia as major environmental problems in coastal marine ecosystems (7)(8)(9). Thus far, fish welfare assessment is still in the infancy state due to the limited understanding of the diverse fish species' welfare-relevant biology (10).…”