Dietary Phytogenics and Galactomannan Oligosaccharides in Low Fish Meal and Fish Oil-Based Diets for European Sea Bass (Dicentrarchus labrax) Juveniles: Effects on Gill Structure and Health and Implications on Oxidative Stress Status

Abstract

An effective replacement for fish meal (FM) and fish oil (FO) based on plant-based raw materials in the feed of marine fish species is necessary for the sustainability of the aquaculture sector. However, the use of plant-based raw materials to replace FM and FO has been associated with several negative health effects, some of which are related to oxidative stress processes that can induce functional and morphological alterations in mucosal tissues. This study aimed to evaluate the effects of dietary oligosaccharides of plant origin (5,000 ppm; galactomannan oligosaccharides, GMOS) and a phytogenic feed additive (200 ppm; garlic oil and labiatae plant extract mixture, PHYTO) on the oxidative stress status and mucosal health of the gills of juvenile European sea bass (Dicentrarchus labrax). The experimental diets, low FM and FO diets (10%FM/6%FO) were supplemented with GMOS from plant origin and PHYTO for 63 days. GMOS and PHYTO did not significantly affect feed utilization, fish growth, and survival. GMOS and PHYTO downregulated the expression of β-act, sod, gpx, cat, and gr in the gills of the fish compared with that in fish fed the control diet. The expression of hsp70 and ocln was upregulated and downregulated, respectively, in the GMOS group compared with that in the control group, whereas the expression of zo-1 was downregulated in the PHYTO group compared with that in the GMOS group. The morphological, histopathological, immunohistochemical, and biochemical parameters of the fish gills were mostly unaffected by GMOS and PHYTO. However, the PHYTO group had lower incidence of lamellar fusion than did the control group after 63 days. Although the tissular distribution of goblet cells was unaffected by GMOS and PHYTO, goblet cell size showed a decreasing trend (−11%) in the GMOS group. GMOS and PHYTO significantly reduced the concentration of PCNA+ in the epithelium of the gills. The above findings indicated that GMOS and PHYTO in low FM/FO-based diets protected the gill epithelia of D. labrax from oxidative stress by modulating the expression of oxidative enzyme-related genes and reducing the density of PCNA+ cells in the gills of the fish.

Effects of cysteine addition to low-fishmeal diets on the growth, anti-oxidative stress, intestine immunity, and Streptococcus agalactiae resistance in juvenile golden pompano (Trachinotus ovatus)

“…Similar findings were made in a previous study on Psetta maxima , which showed that a moderate amount of dietary cysteine (0.3%) enhanced the SGR levels and the mean final weight of P. maxima and improved its growth performance ( 20 ). Oxidative stress and immune capacity reduction caused by low fishmeal content are the main reasons for reduced growth performance ( 8 , 9 , 46 ). In the present study, there were many reasons that cysteine supplementation improved the growth performance of golden pompano in low fishmeal conditions, such as the increased abundance and diversity of gut microbes ( 31 ), increased antioxidant capacity ( 47 , 48 ), and improved immune ability ( 27 ).…”

Gill Oxidative Stress Protection through the Use of Phytogenics and Galactomannan Oligosaccharides as Functional Additives in Practical Diets for European Sea Bass (Dicentrarchus labrax) Juveniles

“…This lack of response in the endogenous antioxidant defenses could be present and associated with the antioxidant properties of the phytogenic compounds, making them capable of inhibiting ROS formation and quenching them once they are formed [ 54 , 55 , 56 ]. Indeed, our previous studies in this mucosal tissue indicated that both functional additives can reduce gill oxidative-stress status in basal conditions after dietary supplementation [ 42 ]. Between the different plant-origin biomolecules, the flavonoids are polyphenolic compounds with high antioxidant properties and can be found in a wide spectrum of plant extracts as garlic oil and labiate plant extracts, such as origanum [ 57 ] and thyme [ 58 ].…”

“…Damage to fish-gill structural integrity like that originated by oxidative-stress processes may lead to degenerative processes such as gas-exchange disturbances [ 61 ] and impairments to immune functions [ 62 ]. In our previous studies, Torrecillas et al (2021) observed the ability of GMOS and PHYTO diets to induce higher gill gene expression of zo-1 and ocln , respectively, in basal conditions [ 42 ]. In the present study, the use of different dietary treatments did not affect fish gill ocln and zo-1 relative gene expression in the early hours after both stress challenges.…”

“…Among the functional ingredients, phytogenic feed additives (PFAs) are plant-derived bioactive compounds such as flavonoids, mucilages, and tannins with antioxidant properties [ 38 , 39 , 40 ]. In previous studies, dietary supplementation with a mixture of garlic and labiate plant essential oils attenuated European sea-bass juveniles’ stress response, with the fish fed the supplemented diets presenting lower circulating cortisol levels in comparison to fish fed a control diet [ 30 , 41 , 42 ]. In addition, PFA supplementation enhanced fish gut-mucosal health, reducing pre-ileorectal valve-segment goblet-cell size as compared to fish fed the control diet [ 41 ].…”

“…Another example of plant-derived functional ingredients are prebiotics, which are indigestible fibers with the ability to enhance host health by selectively stimulating the growth and activity of a limited number of intestinal bacterial species [ 28 , 43 , 44 , 45 , 46 ]. Between them, galactomannan–oligosaccharides (GMOS) have demonstrated in previously reported studies to increase host antioxidant capacity, modulate gut microbiota, and promote gut health in this fish species [ 41 , 42 , 47 ].…”