Skip to main content
SpringerLink
Log in

In vitro evaluation of the effect of a high plant protein diet and nucleotide supplementation on intestinal integrity in meagre (Argyrosomus regius)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

In the present study, the protective effect of nucleotides over damages induced by the consumption of a diet containing a high amount of vegetable ingredients (560 g kg−1) in the intestinal epithelia of the meagre (Argyrosomus regius) was assessed by assays performed with an Ussing-type chamber. Two experimental feeds were prepared including or not a commercial mixture of nucleotides (1 g kg−1). Nucleotides significantly enhanced fish growth during the experiment. On the other hand, differences in the integrity and functionality of intestinal epithelia were evidenced by a change in the polarity of intestinal trans-epithelial potential. Samples of fish fed on the control diet showed a preferentially secretory short-circuit current, while those of fish receiving the nucleotide-supplemented diet showed a significantly lower and preferentially absorptive negative current. It is concluded that alterations of intestinal physiology juvenile meagre resulting from the intake of high amounts of plant ingredients could be minimized by nucleotide supplementation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Baumgart DC, Dignass AU (2002) Intestinal barrier function. Curr Opin Clin Nutr Metab Care 5:685–694

    Article  PubMed  CAS  Google Scholar 

  • Berkes J, Viswanathan VK, Savkovic SD (2003) Intestinal epithelial responses to enteric pathogens: effects on the tight junction barrier, ion transport, and inflammation. Gut 52:439–451

    Article  PubMed  CAS  Google Scholar 

  • Bertelsen LS, Paesold G, Marcus SL, Finlay BB, Eckmann L, Barrett KE (2004) Modulation of chloride secretory responses and barrier function of intestinal epithelial cells by the Salmonella effector protein SigD. Am J Physiol Cell Physiol 287:C939–C948

    Article  PubMed  CAS  Google Scholar 

  • Borda E, Martinez-Puig D, Cordoba X (2003) A balanced nucleotide supply makes sense. Feed Mix 11:24–26

    Google Scholar 

  • Buddington RK, Krogdahl A, Bakke-McKellep AM (1997) The intestines of carnivorous fish: structure and functions and the relations with diet. Acta Physiol Scand Suppl 638:67–80

    PubMed  CAS  Google Scholar 

  • Bueno J, Torres M, Almendros A, Carmona R, Nunez MC, Rios A, Gil A (1994) Effect of dietary nucleotides on small intestinal repair after diarrhea. Histological and ultrastructural changes. Gut 35:926–933

    Article  PubMed  CAS  Google Scholar 

  • Burrells C, William PD, Southage PJ, Wadsworth SL (2001) Dietary nucleotides: a novel supplement in fish feeds 2. Effects on vaccination, salt water transfer, growth rate and physiology of Atlantic salmon. Aquaculture 199:171–184

    Article  CAS  Google Scholar 

  • Clarke LL (2009) A guide to Ussing chamber studies of mouse intestine. Am J Physiol Gastrointest Liver Physiol 296:G1151–G1166

    Article  PubMed  CAS  Google Scholar 

  • Estévez A, Treviño L, Kotzamanis Y, Karacostas I, Tort L, Gisbert E (2011) Effects of different levels of plant protein on the on growing of meagre (Argyrosomus regius) juvenile low temperatures. Aquac Nutr 17(2):338–341

    Article  Google Scholar 

  • Faggio C, Torre A, Lando G, Sabatino G, Trischitta F (2011) Carbonate precipitates and bicarbonate secretion in the intestine of sea bass, Dicentrarchus labrax. J Comp Physiol B181:517–525

    Google Scholar 

  • Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227

    Article  CAS  Google Scholar 

  • Fuentes J, Power DM, Canario AVM (2010) Parathyroid hormone-related protein-stanniocalcin antagonism in regulation of bicarbonate secretion and calcium precipitation in a marine fish intestine. Am Physiol Soc Am J Physiol Regul Integr Comp Physiol 299:R150–R158

    Article  CAS  Google Scholar 

  • Hashimoto K, Matsunaga N, Shimizu M (1994) Effect of vegetable extracts on the transepithelial permeability of the human intestinal Caco-2 cell monolayer. Bioscience. Biotechnol Biochem 58(1994):1345–1346

    Article  Google Scholar 

  • Jutfelt F (2006) The intestinal epithelium of salmonids: trans-epithelial transport, barrier function and bacterial interactions. PhD Thesis, Department of zoology, zoophysiology, Góteborg University, Sweden

  • Knudsen D, Uran P, Arnous A, Koppe W, Frøkiær H (2007) Saponin-containing subfractions of soybean molasses induce enteritis in the distal intestine of Atlantic salmon. J Agric Food Chem 55:2261–2267

    Article  PubMed  CAS  Google Scholar 

  • Knudsen D, Jutfelt F, Sundh H, Sundell K, Koppe W, Frøkiaer H (2008) Dietary soya saponins increase gut permeability and play a key role in the onset of soyabean-induced enteritis in Atlantic salmon (Salmo salar L.). Br J Nutr 100:120–129

    Article  PubMed  CAS  Google Scholar 

  • Krogdahl A, Bakke-McKellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities and pancreatic response in Atlantic salmon (Salmo salar L.). Aquac Nutr 9:361–371

    Article  Google Scholar 

  • Marshall WS, Howard JA, Cozzi RRF, Lynch EM (2002) NaCl and fluid secretion by the intestine of the teleost Fundulus heteroclitus: involvement of CFTR. J Exp Biol 205:745–758

    PubMed  CAS  Google Scholar 

  • Mineo M, Hiroshi H, Norihiro S, Yasuhide O, Fusao T (2002) Melibiose, difructose anhydride III and difructose anhydride IV enhance net calcium absorption in rat small and large intestinal epithelium by increasing the passage of tight junctions in vitro. Nutrient interactions and toxicity. J Nutr 132:3394–3399

    PubMed  CAS  Google Scholar 

  • Pessi T, Sutas Y, Marttinen A, Isolauri E (1998) Probiotics reinforce mucosal degradation of antigens in rats: implications for therapeutic use of probiotics. J Nutr 128:2313–2318

    PubMed  CAS  Google Scholar 

  • Poli BM, Parisi G, Zamapacavall G, Iurzan F, Mecatti M, Lupi P, Bonelli A (2003) Preliminary results on quality and quality changes in reared meagre (Argyrosomus regius): body and fillet traits and freshness changes in refrigerated commercial-size fish. Aquac Int 11:301–311

    Article  Google Scholar 

  • Pratoomyot J, Bendiksen EÅ, Bell JG, Tocher DR (2010) Effects of increasing replacement of dietary fishmeal with plant protein sources on growth performance and body lipid composition of Atlantic salmon (Salmo salar L.). Aquaculture 305:124–132

    Article  CAS  Google Scholar 

  • Robaina L, Izquierdo MS, Moyano FJ, Socorro J, Vergara JM, Montero D, Fernández-Palacios H (1995) Soybean and lupin seed meals as protein sources in diets for gilthead seabream (Sparus aurata): nutritional and histological implications. Aquaculture 130:219–233

    Article  Google Scholar 

  • Santigosa E, Sánchez J, Médale F, Kaushik S, Pérez-Sánchez J, Gallardo MA (2008) Modifications of digestive enzymes in trout (Oncorhynchus mykiss) and sea bream (Sparus aurata) in response to dietary fish meal replacement by plant protein sources. Aquaculture 282:68–74

    Article  CAS  Google Scholar 

  • Schroede B, Duncker S, Barth S, Bauerfeind R, Gruber AD, Deppenmeier S, Breves G (2006) Preventive effects of the probiotic Escherichia coli strain Nissle 1917 on acute secretory diarrhea in a pig model of intestinal infection. Dig Dis Sci 51(4):724–731

    Article  Google Scholar 

  • Sundella K, Jutfelta F, Agustsson T, Olsenc RE, Sandbloma E, Hansenc T, Bjornssona BT (2003) Intestinal transport mechanisms and plasma cortisol levels during normal and out-of-season parr–smolt transformation of Atlantic salmon, Salmo salar. Aquaculture 222:265–285

    Article  Google Scholar 

  • Tacon AGJ, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285:146–158

    Article  CAS  Google Scholar 

  • Thiel-Demby VE, Humphreys JE, John-Williams LA, Ellens HM, Shah N, Ayrton AD, Polli JW (2009) Biopharmaceutics classification system: validation and learnings of an in vitro permeability assay. Mol Pharm 6:11–18

    Article  PubMed  CAS  Google Scholar 

  • Torstensen BE, Bell G, Rosenlund GR, Henderson J, Graff IE, Tocher DR, Lie O, Sargent JR (2005) Tailoring of Atlantic salmon (Salmo salar) flesh lipid composition and sensory quality by replacing fish oil with a vegetable oil blend. J Agric Food Chem 53:10166–10178

    Article  PubMed  CAS  Google Scholar 

  • Torstensen BE, Espe M, Sanden M, Stubhaug I, Waagbo R, Hemre GI, Fontanillas R, Nordgarden U, Hevroy EM, Olsvik P, Berntssen MHG (2008) Novel production of Atlantic salmon (Salmo salar) protein based on combined replacement of fish meal and fish oil with plant meal and vegetable oil blends. Aquaculture 285:193–200

    Article  CAS  Google Scholar 

  • Trischitta F, Faggio C (2006) Effect of the flavonol quercetin on ion transport in the isolated intestine of the eel, Anguilla anguilla. Comp Biochem Physiol C 143:17–22

    Google Scholar 

  • Trischitta F, Faggio C (2008) Gossypol affects ion transport in the isolated intestine of the seawater adapted eel, Anguilla anguilla. Comp Biochem Physiol A 151:139–143

    Google Scholar 

Download references

Acknowledgments

To BIOIBERICA and to SPAROS for providing, respectively, the nucleotides and the diets used in this research. To Fundación Alfonso Martín Escudero for supporting M. A. Saenz de Rodrigáñez, with a postdoctoral fellowship. This research used resources from project PTDC/MAR/104008/2008 (Ministry of Science and Higher Education, Portugal and European Social Funds), PROMAR projects (AQUACOR 31-03-05FEP-003 and NUTRICOR 31-03-05-FEP-19, co-financed by FEDER.) and FCT-“Ciência 2008 program”.

Author information

Authors and Affiliations

  1. Aquaculture Research Station, IPMA - Portuguese Institute for the Sea and Atmosphere, Av. 5 de Outubro, s/n, 8700-305, Olhão, Portugal

    M. A. Sáenz de Rodrigáñez & L. Ribeiro

  2. Center of Marine Sciences, CIMAR-LA, University of Algarve, Campus de Gambelas, 8005-139, Faro, Portugal

    J. Fuentes

  3. Department of Applied Biology, University of Almería, 04120, Almería, Spain

    F. J. Moyano

Authors
  1. M. A. Sáenz de Rodrigáñez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Fuentes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. J. Moyano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. A. Sáenz de Rodrigáñez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Rodrigáñez, M.A.S., Fuentes, J., Moyano, F.J. et al. In vitro evaluation of the effect of a high plant protein diet and nucleotide supplementation on intestinal integrity in meagre (Argyrosomus regius). Fish Physiol Biochem 39, 1365–1370 (2013). https://doi.org/10.1007/s10695-013-9790-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-013-9790-x

Keywords

Search

Navigation