Improved glucose and lipid metabolism in European sea bass (Dicentrarchus labrax) fed short-chain fructooligosaccharides and xylooligosaccharides

Highlights

• First study about prebiotics and glucose metabolism in fish

• XOS decreased lipogenesis and improved fish growth performance.

• XOS and scFOS increased glycolytic activity in fish fed fish meal diets.

• XOS and scFOS improve glucose and lipid metabolism in European sea bass.

Abstract

The effects of short-chain fructooligosaccharides (scFOS) and xylooligosaccharides (XOS) on growth, feed utilization and liver activity of key enzymes of glycolytic, gluconeogenic, and lipogenic pathways were studied in European sea bass juveniles. This is the first study about the effect of prebiotics on fish glucose metabolism and few and contradictory studies are available about prebiotic effect on lipid metabolism.

Fish were fed isoproteic (46%) and isolipidic (15%) diets based on fish meal (FM diets) or plant ingredients (PP diets; 30 FM:70 PP) as main protein sources. Four other diets were formulated similar to the control diets (PPC; FMC) but including 1% scFOS or 1% XOS (PPFOS, PPXOS, FMFOS and FMXOS diets). Growth performance was higher in fish fed PPXOS diet than PPC diet. No effect of dietary prebiotics on feed efficiency was noticed. Glucokinase activity was higher in fish fed FMFOS and FMXOS diets than FMC diet. Lipogenic enzyme activities (malic enzyme, fatty acid synthetase, glucose-6-phosphate dehydrogenase) were lower in fish fed diets including XOS than in the other groups. Glycolytic (glucokinase, pyruvate kinase) and lipogenic enzyme activities were higher, and gluconeogenic (fructose-1,6-bisphosphatase) enzyme activity was lower in fish fed FM diets than the PP diets. Overall, dietary XOS decreased lipogenesis, independently of dietary protein source, and improved growth performance in fish fed PP diets. In fish fed FM diets, XOS and scFOS increased glycolytic activity. XOS seemed to have good potential to be used as prebiotic in European sea bass.

Introduction

Prebiotics by definition are non-digestible feed ingredients that beneficially affect the host by selectively stimulating the growth and/or activity of specific bacteria present in the gastrointestinal tract (GI), improving host health (Gibson and Roberfroid, 1995). Therefore prebiotics are selectively fermented by specific-health promoting bacteria such as Lactobacillus and Bifidobacterium, leading to a decrease of pathogenic bacterial species in the GI tract and/or to the production of fermentation end products, mainly short-chain fatty acids (SCFAs), which can modulate host glucose and lipid metabolism (Delzenne et al., 2008, Gibson and Roberfroid, 1995, Qiang et al., 2009, Roberfroid et al., 2010). Compared with humans and farm animals, less information is available concerning the effects of prebiotics on aquatic animals (Dimitroglou et al., 2011, Merrifield et al., 2010, Ringø et al., 2010).

Fructooligosaccharides (FOS) are among the most well-established prebiotics for use in aquafeeds (Ringø et al., 2010). FOS are produced on a commercial scale by two different processes, either through enzymatic hydrolysis of chicory-root inulin or from sucrose. FOS are composed by long linear chains of fructose units linked by β-(2–1) bonds attached to a terminal glucose unit. Short-chain fructooligosaccharides (scFOS) have a chemical composition similar to that of FOS but a degree of polymerization of only 1 to 5 glucose units (Bornet et al., 2002). FOS are fermented in the GI tract by beneficial bifidobacteria and other lactic-acid producing bacteria which possess β-fructosidase that hydrolyses β-(2–1) glycosidic bonds, an enzyme lacking in mammals and fish digestive tracts (Roberfroid and Slavin, 2000). In several fish species, it was reported that FOS and scFOS improved growth performance and feed efficiency, enhanced non-specific immune responses and disease resistance, improved gut function and morphological status, and increased health-promoting bacteria in the intestine (Anguiano et al., 2013, Hui-yuan et al., 2007, Ortiz et al., 2013, Soleimani et al., 2012, Zhou et al., 2009, Zhou et al., 2010).

Xylooligosaccharide (XOS) is an emerging prebiotic gaining importance as functional ingredient in pharmaceutics, feed and food formulation (Aachary and Prapulla, 2011). Industrially, XOS is produced by chemical or enzymatic hydrolysis of xylan, which is the major component of lignocellulosic raw materials (Vázquez et al., 2000). Although the chemical structure of XOS depends on the xylan source, it generally consists of chains of xylose linked by β-(1–4) bonds, with a degree of polymerization ranging from 2 to 10. Studies in mammals showed that XOS promoted activity of beneficial intestinal bacteria, mainly Bifidobacterium species, leading to an increase of caeca SCFAs (Broekaert et al., 2011). These two effects are related with a number of health benefits, including improvement of bowel function, mineral absorption, lipid and glucose metabolism, immunomodulatory activity, reduction of colon cancer risk, and to antioxidant, anti-inflammatory and anti-microbial functions (Aachary and Prapulla, 2011, Broekaert et al., 2011). Up to now, only two studies were performed to evaluate XOS potential in fish (Li et al., 2008, Xu et al., 2009). In allogynogenetic crucian carp (Carassius auratus gibelio) growth performance and digestive enzyme activities were higher in fish fed 100 mg XOS kg^− 1 compared to the control diet (Xu et al., 2009). Dietary XOS incorporation at 400 mg kg^− 1 enhanced growth performance and nonspecific immunity of juvenile turbot (Scophthalmus maximus) (Li et al., 2008).

It has been reported that prebiotics, namely FOS and XOS, can alter glucose and lipid metabolism in mammals, depending on colonic fermentation process (Broekaert et al., 2011, Delzenne et al., 2008, Roberfroid et al., 2010). Thus, several studies indicated that FOS and XOS improved glucose tolerance, by lowering plasma glucose levels and enhancing insulin sensitivity (Gobinath et al., 2010, Respondek et al., 2011, Sheu et al., 2008, Shinoki and Hara, 2011), and reduced hepatic lipogenesis, serum and liver cholesterol, and triacylglycerides levels and increased serum HDL/LDL ratio (Fiordaliso et al., 1995, Kok et al., 1996, Sheu et al., 2008, Wang et al., 2011). However, the effect of prebiotics on lipid metabolism in fish was scarcely studied (Guerreiro et al., 2014, Torrecillas et al., 2011b) and no studies are available concerning prebiotic effects on glucose metabolism.

In contrast to probiotics, few studies on prebiotic effects were conducted in European sea bass (Dicentrarchus labrax), and focused only on the effect of mannanoligosaccharides (MOS) on the immune system and disease resistance (Torrecillas et al., 2007, Torrecillas et al., 2011a, Torrecillas et al., 2011b, Torrecillas et al., 2012, Torrecillas et al., 2013). The aim of the present study was thus to assess the role of scFOS and XOS, incorporated into plant protein or fish meal based diets, on European sea bass glucose and lipid metabolism, through measurement of activities of key liver enzymes of glycolytic, gluconeogenic and lipogenic pathways.