Improving growth potential in Senegalese sole (Solea senegalensis) through dietary protein

doi:10.1016/j.aquaculture.2018.08.044

Aquaculture

Volume 498, 1 January 2019, Pages 90-99

https://doi.org/10.1016/j.aquaculture.2018.08.044 Get rights and content

Highlights

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Manipulating dietary protein quality or complexity had different effects on sole larvae capacity to utilize and retain protein.
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Changing dietary IAA/DAA ratio or protein complexity affected myogenesis, which reflected on sole somatic growth potential.
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More than dietary AA profile, changing dietary protein complexity shows as a promising way to improve growth in sole early larvae.
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Dietary protein formulation of microdiets for Senegalese sole should be adapted to each developmental stage.

Abstract

In the present work, recent studies that contributed for improving dietary protein in practical microdiets for Senegalese sole larvae are revised, in an attempt to overcome some of the current problems in this species larviculture, such as the difficult early adaptation to inert diets and highly variable growth rates. Different diet formulation strategies were employed in an attempt to improve Senegalese sole larvae capacity to utilize and deposit protein throughout metamorphosis, to further maximize growth potential: (1) increasing indispensable amino acids (IAA) content; (2) meeting the ideal IAA profile by adjusting the dietary AA profile to the larval body AA profile; and (3) decreasing the complexity (molecular weight) of dietary protein to increase its digestibility. Either manipulating the quality or the complexity of dietary protein had impact on the larvae capacity to utilize protein and direct it for growth. Sole larvae seem to be able to adapt their digestive functions and metabolic capacity to dietary protein. Moreover, increasing the dietary IAA/DAA ratio and changing the degree of hydrolysis of dietary protein affected the expression pattern of muscle growth related genes, with consequences on muscle cellularity and potential for growth. The expression of DNA methyltransferases was altered in response to changes in dietary protein. The novelty of such information in fish may trigger further studies on the effect of dietary protein on the epigenetic regulation of growth.

In conclusion, optimal protein quality for Senegalese sole seems to change during larval development. Whereas the inclusion of a moderately hydrolysed protein comes up as a promising way to improve growth in early larval stages, larger peptides and intact protein seem to be more suitable to sole post-larvae and young juveniles. Therefore, these results suggest that dietary protein fraction formulation of microdiets for Senegalese sole should be adapted to each developmental stage, what has important consequences for practical larval microdiets formulation and feeding protocols.

Introduction

Senegalese sole is a robust fast-growing species mostly reared in Portugal and Spain and more recently in France and Italy (FEAP, 2016). The larviculture protocols were successfully established by Dinis et al., 1999, and are nowadays fairly standardized, with post-larvae being routinely produced with good growth and at high survival rates (Morais et al., 2016). However, until recently, some problems have hampered a more successful juvenile production, such as difficulties in weaning, variable growth rates and large size dispersion, which might be related to suboptimal rearing or nutritional conditions during early life stages (Morais et al., 2016).

Due to a growing knowledge on Senegalese sole physiology and recent technological developments, sole production is going through an important expansion: total production of farmed sole has risen from 68 to 1457 t in the period 2007–2015 in Europe (FEAP, 2016). This will inevitably lead to an increase in the demand for high quality juvenile production. This prospective scenery makes it urgent to increase Senegalese sole larvae and juvenile quality, which may be pursued by improving early larvae nutrition.

Live feed nutritional composition is considered as sub-optimal for Senegalese sole larvae on what concerns protein quality (Aragão et al., 2004a, Aragão et al., 2004b) and that has been suggested as a possible cause for the variable growth rates. Using a microdiet to supplement live feed in a co-feeding regime or an earlier weaning have been pointed as possible solutions to overcome the inadequacy of the commonly cultivated zooplantonic species to sole nutritional needs (Engrola et al., 2009). In order to do so, a suitable microdiet must be developed to meet these larvae nutritional needs.

The basis for formulating a commercial microdiet to be introduced from an early stage (first feeding) to Senegalese sole have been set mostly in the last 15 years (reviewed by Conceição et al., 2007; Morais et al., 2016; Engrola et al., 2018; Pinto et al., 2018). Recent projects have largely contributed to the development of commercial microdiets for several flatfish species that showed to be suitable for a successful weaning of Senegalese sole post-larvae (Portuguese projects MICALA, 2010–2012 13,380/QREN, SOLEAWIN 2014–2015 310,305/FEP/71, and EPISOLE PTDC/MAR/110547/2009). A sudden weaning may be achieved at 25-30DAH, and the only significant remaining problem is a large size dispersion. So, there is room for improving the current commercial microdiets and anticipate sudden weaning or to eventually supplement or even definitely replace live feeds at mouth opening.

Section snippets

The role of protein synthesis

Fish growth is mainly driven by protein deposition (Houlihan et al., 1995; Shearer, 1994) and maximal protein deposition and associated carcass lean growth rate determine the nutrient requirements for growth (Schinckel and de Lange, 1996).

Protein deposition or accretion is the net result of the dynamic balance between protein synthesis and protein degradation, in a process called protein turnover (Millward et al., 1975). Protein turnover is the continuous renewal and cycling of tissue proteins

Somatic growth potential and muscle growth

Fish larvae have an allometric growth, with the relative contribution of white muscle increasing throughout development when compared to other tissues, such as liver and the digestive tract (Dabrowski, 1986). Therefore, the efficiency of protein retention and synthesis in skeletal muscle is probably a major determinant of larvae dietary AA requirements throughout development. In fact, skeletal muscle protein deposition was suggested to greatly contribute to overall growth in fish and fish

Dietary protein and epigenetics

It has been recently suggested that an epigenetic event could promote differential gene expression and modulate Senegalese sole muscle growth in response to different rearing temperatures (Campos et al., 2013a). Epigenetic events induce potentially reversible modification of DNA, though not involving modification in the underlying DNA sequence (Berger et al., 2009). Such events occur throughout life and can be influenced by external factors (Anderson et al., 2012). Thus, external effects on the

Dietary effect on protein metabolism and somatic growth

Different diet formulation strategies have been employed to meet the IAA requirements of Senegalese sole larvae so to improve their capacity to utilize and deposit protein throughout metamorphosis and maximize growth potential. In Canada et al. (2016a), dietary protein quality was manipulated by adjusting the dietary AA profile to the larval body AA profile, through a 4% supplementation with encapsulated CAA (Fig.1). This strategy had a positive short-term effect on sole larvae capacity to

Dietary effect on protein metabolism and somatic growth

In Canada et al. (2017), dietary protein complexity was manipulated to improve its digestibility, by including protein hydrolysates with different molecular weights. When comparing a diet mostly based on native protein sources (Intact), a diet mostly based on low MW peptides (<5KDa, HighH), and a diet mostly based on polypeptides ranging from 5 to 70 KDa (PartH), the later promoted growth in metamorphosing larvae (Canada et al., 2017) (Fig.4), which digestive system is still very immature, with

Conclusions

Manipulating dietary protein quality upon different concepts or dietary protein complexity had different effects on the development of the larvae capacity to utilize and retain protein for growth purposes. Changing either the dietary IAA/DAA ratio or protein complexity exerted a strong influence on sole larvae muscle development, by inducing changes in the myogenic processes that were reflected on somatic growth potential. The dietary induced changes in myogenesis were variable: either delayed

Acknowledgements

This work was funded by the Project EPISOLE (FCT) [PTDC/MAR/110547/2009], through project UID/Multi/04326/2013 (Portugal) from FCT (Portugal), and by the project MICALA — I&DT Co-Promoção No. 13380 (Portugal, supported by POAlgarve 21, QREN and European Union). P. Canada was supported by FCT grant SFRH/BD/82149/2011. S. Engrola was supported by FCT investigator grant IF/00482/2014/CP1217/CT0005 funded by the European Social Fund, the Operational Programme Human Potential and the Foundation for

Conflict of interest

The authors declare that they have no conflict of interest.

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ReviewImproving growth potential in Senegalese sole (Solea senegalensis) through dietary protein

Highlights

Abstract

Introduction

Section snippets

The role of protein synthesis

Somatic growth potential and muscle growth

Dietary protein and epigenetics

Dietary effect on protein metabolism and somatic growth

Dietary effect on protein metabolism and somatic growth

Conclusions

Acknowledgements

Conflict of interest

J. Nutr. Biochem.

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Gene

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Biochemistry & molecular biology.

Aquaculture

Aquaculture

Aquaculture

Aquaculture

Aquaculture

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Mar. Genomics

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Aquaculture

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Brain Res.

J. Hepatol.

Biochemistry & molecular biology.

Gen. Comp. Endocrinol.

Aquaculture

Aquaculture

Biochemistry & molecular biology.

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Physiol. Behav.

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Growth characteristics of skeletal muscle tissue in Oreochromis niloticus larvae fed on a lysine supplemented diet

J. Fish Biol.

Growth and multiplication of white skeletal muscle fibres in carp larvae in relation to somatic growth rate

J. Fish Biol.

Early decrease in dietary protein:energy ratio by fat addition and ontogenetic changes in muscle growth mechanisms of rainbow trout: short- and long-term effects

Br. J. Nutr.

Maternal dietary protein restriction and excess affects offspring gene expression and methylation of non-SMC subunits of condensin I in liver and skeletal muscle

Epigenetics

A purified test diet for coho salmon, Oncorhynchus kisutch, fry

Bull. Jpn. Soc. Sci. Fish.

Review
Improving growth potential in Senegalese sole (Solea senegalensis) through dietary protein