Redox Challenge in a Cultured Temperate Marine Species During Low Temperature and Temperature Recovery

Abstract

Aquaculture is a growing industry that is increasingly providing a sizable proportion of fishery products for human consumption. Dietary energy and temperature fluctuations affect fish health and may even trigger mortality, causing great losses in fish production during winter. To better understand this unproductive winter period in aquaculture, the redox status in a cultured marine species, the gilthead sea bream, was analyzed for the first time by inducing controlled temperature fluctuations and reducing dietary lipid content. Two groups of fish (by triplicate), differing in their dietary lipid content (18% vs. 14%), were subjected to 30 days at 22°C (Pre-Cold), 50 days at 14°C (Cold) and then 35 days at 22°C (Recovery). Plasma and liver redox metabolites (oxidized lipid, oxidized protein and thiol groups), liver glutathione forms (total, oxidized and reduced) and liver antioxidant enzyme activities were measured. Reducing dietary lipid content did not affect gilthead sea bream growth, glutathione levels or enzyme activities, but did reduce the amount of oxidized lipids. A sustained low temperature of 14°C showed a lack of adaptation of antioxidant enzyme activities, mainly catalase and glutathione reductase, which subsequently affected the glutathione redox cycle and caused an acute reduction in total hepatic glutathione levels, irrespective of diet. Antioxidant enzyme activities were gradually restored to their pre-cold levels, but the glutathione redox cycle was not restored to its pre-cold values during the recovery period used. Moreover, the lower lipid diet was associated with transiently increased liver oxidized protein levels. Thus, we propose that fish should be fed a low lipid diet during pre-cold and cold periods, which would reduce oxidized lipid levels without affecting fish growth, and a higher energy diet during the recovery period. Moreover, diets supplemented with antioxidants should be considered, especially during temperature recovery.

Modulation of Pituitary Response by Dietary Lipids and Throughout a Temperature Fluctuation Challenge in Gilthead Sea Bream

“…Gene expression of growth hormone, a major pituitary maker for growth and satiation, was reduced by feeding energetic restriction in cultured Labeo rohita [31], and in the present study, gh expression was up-regulated when the fish were fed diet D18, which is in agreement with the increased circulating levels of gh observed in gilthead fingerlings fed with 17% lipid with respect to 9% [32]. However, in the present case and contrary to those studies, the change in gh expression did not result in significant changes in the analysed growth parameters during this 30-day period [8]. Growth hormone actions are mediated by the Insulin growth factor 1 (IGF-1), which was not evaluated in relation to diet.…”

“…Glucocorticoid receptor gr expression in sea bream has been suggested to be tissue specific and correlated to plasma cortisol levels [46]. This could not be the case in our pre-cold conditions, where a change in total dietary lipid of 4% did not prove to be a stressor condition [8,16]. As reported for pituitary modulation by amino acid supplementation [29], dietary lipids were also recognized as conditioning pituitary function by the expression of both the hormones and receptors studied.…”

“…In the case of gilthead sea bream, reducing dietary lipid before the cold season has been proposed to cope with liver affectations [4,[26][27][28]. We previously demonstrated that reducing dietary lipid from 18% to 14% resulted in a similar body weight, condition factor, SGR (0.86 ± 0.05 for D14 and 0.97 ± 0.05 for D18) and FCR (1.32 ± 0.02 for D14 and 1.33 ± 0.06 for D18) (data from [16]), with an improved redox status [8,16], suggesting a more efficient metabolism when sea bream have been fed a low lipid diet. The study of pituitary function during the pre-cold period showed that dietary lipid intake is capable of modifying pituitary expression of gh, tsh and both pomc hormones, together with that of the receptors trβ and gr.…”

“…Thus, although the changes in gene transcription at the pituitary level in relation to feed energy are important, it is not clear if they may result in altered hormone secretion and overall impact. To better elucidate the peripheral effects (growth and plasma markers) of dietary lipids proposed in the current trial, we performed a PCA analyses ( Figure 5) of body performance data, such as body weight, body length, condition factor and hepatosomatic index [8] together with relevant plasma metabolites markers such as glucose, lactate, and lipid fractions (NEFA and TAG) [16]. Similarly to thyroid hormone levels, we observed that both body parameters and plasma metabolites such as glucose, lactate or proteins did not show differences after overnight fasting for fish fed 18% or 14% dietary lipids [8,16], and resulting PCA did not discriminate between D14 or D18, differently to above-mentioned greater differences in pituitary expression.…”

“…The pituitary receptors selected were the glucocorticoid receptor (GR), and thyroid receptors (TRα and TRβ). Moreover, levels in plasma thyroid hormones T 3 and T 4 were also measured and taken in account together with known data on growth [8] and plasma metabolites [16] via principal components analyses (PCA).…”