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Specific Features of Nutrient Transport in the Digestive Tract of Fish

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Abstract

The review briefly addresses the mechanisms underlying micro- and macromolecular transport of proteins, fats and carbohydrates in the fish intestines. A special focus is on the differences between some mechanisms of micromolecular transport of peptides, amino acids and hexoses, as well as craniocaudal transport gradients, in fish compared to mammals. Transport proteins emerge at the earliest stages of fish ontogenesis, before the transition of fish larvae to exogenous feeding. The reasons behind the differences in the intestinal transport systems are analyzed.

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REFERENCES

  1. Membrannyi gidroliz i transport. Novye dannye i gipotezy (Membrane Hydrolysis and Transport. New Data and Hypotheses), Ugolev, A.M., Ed., Leningrad, 1986.

  2. Metelsky, S.T., Transportnye protsessy i membrannoe pishchevarenie v tonkoi kishke. Elektrofiziologicheskaya model (Transport Processes and Membrane Digestion in the Small Intestine. Electrophysiological Model), Moscow, 2007.

  3. Ugolev, A.M. and Kuzmina, V.V., Pishchevaritelnye protsessy i adaptatsii u ryb (Digestive Processes and Adaptations in Fish), St. Petersburg, 1993.

  4. Kuzmina, V.V., Fiziologo-biokhimicheskie osnovy ekzotrofii ryb (Physiological and Biochemical Foundations of Fish Exotrophy), Moscow, 2005.

  5. Kuzmina, V.V., Protsessy pishchevareniya u ryb. Novye fakty i gipotezy (Digestive Processes in Fish. New Facts and Hypotheses), Yaroslavl, 2018.

  6. Ferraris, R.P. and Ahearn, G.A., Sugar and amino acid transport in fish intestine, Comp. Biochem. Physiol. A, 1984, vol. 77(3), pp. 397–413.

  7. Golovanova, I.L. and Kuzmina, V.V., Transport of nutrients in the intestines of fish, Biol. Vnutr. Vod, 1998, vol. 2, pp. 62–72.

  8. Rønnestad, I. and Morais, S.J., Digestion, Fish Larval Physiology, Finn, R.N. and Kapoor, B.G., Eds., USA Enfield, New Hampshire, 2008, pp. 201–262.

  9. Bakke, A.M., Glover, Ch., and Krogdahl, A., Feeding, digestion and absorption of nutrients, Fish Physiology. The Multifunctional Gut of Fish, Grosell, M., Farrell, A.P., and Brauner, C.J., Eds., Amsterdam, Boston, 2011, vol. 30, pp. 57–110.

  10. Verri, T., Barca, A., Pisani, P., Piccinni, B., Storelli, C., and Romano, A., Di- and tripeptide transport in vertebrates: the contribution of teleost fish models, J. Comp. Physiol., 2016, vol. 187(3), pp. 395–462. https://doi.org/10.1007/s00360-016-1044-7

  11. Ferraris, R.P., Does glucose uptake in marine fish intestines occur by active transport? Pasif. Sci., 1982, vol. 36(4), pp. 510–522.

  12. Collie, N.L. and Ferraris, R.P., Nutrient fluxes and regulation in fish intestine, Metabolic Biochemistry. Biochemistry and Molecular Biology of Fishes Series, Hochachka, P.W. and Mommsen, T.P., Eds., Amsterdam, vol. 4, pp. 221–239.

  13. Verri, T., Kottra, G., Romano, A., Tiso, N., Peric, M., Maffia, M., Boll, M., Argenton, F., Daniel, H., and Storelli, C., Molecular and functional characterization of the zebrafish (Danio rerio) PEPT1-type peptide transporter, FEBS Letters, 2003, vol. 549, pp. 115–122.

  14. Con, P., Nitzan, T., Slosman, T., Harpaz, S., and Cnaani, A., Peptide transporters in the primary gastrointestinal tract of pre-feeding Mozambique tilapia larva, Front. Physiol., 2019. https://doi.org/10.3389/fphys.2019.00808

  15. Ash, R. and McLean, E., Intact protein absorption in teleost: comparative consideration, Arсh. Int. Physiol. Biochem., 1989, vol. 97(5), pp. 51–70.

  16. Sire, M.-F., Dorin, D., and Vernier, J.-M., Intestinal absorption of macromolecular proteins in rainbow trout, Aquacult., 1992, vol. 100, pp. 234–235.

  17. Bakke-McKellep, A.M., Nordrum, S., Krogdahl, Å., and Buddington, R.K., Absorption of glucose, amino acids, and dipeptides by the intestines of Atlantic salmon (Salmo salar L.), Fish Physiol. Biochem., 2000, vol. 22, pp. 33–44.

  18. Concha, M.I., Santander, C.N., Villanueva, J., and Amthauer, R., Specific binding of the endocytosis tracer horseradish peroxidase to intestinal fatty acid-binding protein (I-FABP) in apical membranes of carp enterocytes, J. Exp. Zool., 2002, vol. 293, pp. 541–550.

  19. Valle, A.Z., Iriti, M., Faoro, F., Berti, C., and Ciappellano, S., In vivo prion protein intestinal uptake in fish, Acta Pathol. Microbiol. Immunol. Scand., 2008, vol. V, pp. 173–180.

  20. Deplano, M., Connes, R., Diaz, J.P., and Barnabe, G., Variation in the absorption of macromolecular protein in larvae of the sea bass (Dicentrarchus labrax) during transition to the exotrophic phase, Mar. Biol., 1991, vol. 110, pp. 29–36.

  21. Thamotharan, M., Gomme, J., Zonno, V., Maffia, M., Storelli, C., and Ahearn, G.A., Electrogenic, proton-coupled, intestinal dipeptide transport in herbivorous and carnivorous teleosts, Amer. J. Physiol., 1996, vol. 270, R939–R947. https://doi.org/10.1152/ajpregu.270.5.R939.1996

  22. Ugolev, A.M., Kuzmina, V.V., Roshchina, G.M., Smirnova, L.F., Golovanova, I.L., and Gruzdkov, A.A., Characteristics of membrane hydrolysis and transport in fish, Izv. Akad. Nauk SSSR, Ser. Biol., 1989, vol. 3, pp. 341–349.

  23. Boge, G., Rigal, A., and Peres, G., Rates of in vivo intestinal absorption of glycine and glycylglycine by rainbow trout (Salmo gairdneri Richardson), Comp. Biochem. Physiol., 1981, vol. 69(3), pp. 455–459.

  24. Vilella, S., Ahearn, G.A., Cassano, G., and Storelli, C., Na-dependent L-proline transport by ell intestinal brush-border membrane vesicles, Amer. J. Physiol., 1988, vol. 255(4), Pt. 2, pp. R648–R653.

  25. Farmafarmaian, A.A., Ross, A., and Mazal, A., In vivo intestinal absorption of sugar in the toadfish (marine teleost, Opsanus tau), Biol. Bull., 1972, vol. 142, pp. 427–445.

  26. Kuzmina, V.V. and Izvekova, G.I., Mechanisms of carbohydrate transport in the intestines of freshwater teleost fishes, Biol. Vnutr. Vod. Inform. Bull., 1988, vol. 79, pp. 42–44.

  27. Storelli, C., Vilella, S., Romano, A., Maffia, M., and Cassano, G., Brush-border amino acid transport mechanisms in carnivorous eel intestine, Am. J. Physiol., 1989, vol. 257, pp. R506–R510.

  28. Boge, G., Roche, H., and Balocco, C., Amino acid transport by intestinal brush border vesicles of a marine fish, Boops salpa, Comp. Biochem. Physiol., 2002, vol. 131B, pp. 19–26.

  29. Verri, T., Romano, A., Barca, A., Kottra, G., Daniel, H., and Storelli, C., Transport of di- and tripeptides in teleost fish intestine, Aquacult. Res., 2010, vol. 41, pp. 641–653. https://doi.org/10.1111/j.1365-2109.2009.02270.x

  30. Romano, A., Kottra, G., Barca, A., Tiso, N., Maffia, M., Argenton, F., Daniel, H., Storelli, C., and Verri, T., High-affinity peptide transporter PEPT2 (SLC15A2) of the zebrafish Danio rerio: functional properties, genomic organization, and expression analysis, Physiol. Genom., 2006, vol. 24, pp. 207–217.

  31. Gonçalves, A.F., Castro, L.F.C., Pereira-Wilson, C., Coimbra, J., and Wilson, J.M., Is there a compromise between nutrient uptake and gas exchange in the gut of Misgurnus anguilli caudatus, an intestinal air-breathing fish? Comp. Biochem. Physiol., 2007, vol. 2D, pp. 345–355.

  32. Hakim, Y., Harpaz, S., and Uni, Z., Expression of brush border enzymes and transporters in the intestine of European sea bass (Dicentrarchus labrax) following feed deprivation, Aquacult., 2009, vol. 290, pp. 110–115.

  33. Sangaletti, R., Terova, G., Peres, A., Bossi, E., Cora, S., and Saroglia, M., Functional expression of the oligopeptide transporter PepT1 from the sea bass (Dicentrarchus labrax), Pflügers Arch. (Eur. J. Physiol.), 2009, vol. 459, pp. 47–54.

  34. Terova, G., Cora, S., Verri, T., Rimoldi, S., Bernardini, G., and Saroglia, M., Impact of feed availability on PepT1 mRNA expression levels in sea bass (Dicentrarchus labrax), Aquacult., 2009, vol. 294, pp. 288–299.

  35. Bakke, S., Jordal, A.-E.O., Gómez-Requeni, P., Verri, T., Kousoulaki, K., Aksnes, A., and Rønnestad, I., Dietary protein hydrolysates and free amino acids affect the spatial expression of peptide transporter PepT1 in the digestive tract of Atlantic cod (Gadus morhua), Comp. Biochem. Physiol. B, 2010, vol. 156, pp. 48–55. https://doi.org/10.1016/j.cbpb.2010.02.002

  36. Ostaszewska, T., Kamaszewski, M., Grochowski, P., Dabrowski, K., Verri, T., Aksakal, E., Muszynska, M., Nowak, Z., and Dobosz, S., The effect of peptide absorption on PepT1 gene expression, and digestive system hormones in rainbow trout (Oncorhynchus mykiss Walbaum, 1792), Comp. Biochem. Physiol. A, 2010, vol. 155, pp. 107–114. https://doi.org/10.1016/j.cbpa.2009.10.017

  37. Ahn, H., Yamada, Y., Okamura, A., Tsukamoto, K., Kaneko, T., and Watanabe, S., Intestinal expression of peptide transporter 1 (PEPT 1) at different life stages of Japanese eel, Anguilla japonica, Fish Physiol. Biochem. B, 2013, vol. 166(2), pp. 157–164. https://doi.org/10.1016/j.cbpb.2013.08.005PMID:23994609

  38. Vilella, S., Ahearn, G.A., Cassano, G., and Storelli, C., How many Na+-dependent carriers for L-alanine and L-proline in the eel intestine? Studies with brush border membrane vesicles, Biochim. Biophys. Acta, 1989, vol. 984, pp. 188–192.

  39. Glover, C.N., Bucking, С., and Wood, C.M., Characterization of L-alanine and glycine absorption across the gut of an ancient vertebrate, Comp. Biochem. Physiol. B, 2011, vol. 166(2), pp. 157–164.

  40. Glover, C.N. and Wood, C.M., Histidine absorption across apical surfaces of freshwater rainbow trout intestine: mechanistic characterization and the influence of copper, J. Membr. Biol., 2008, vol. 221, pp. 87–95.

  41. Applebaum, S.L. and Rоnnestad, I., Absorption, assimilation and catabolism of individual free amino acids by larval Atlantic halibut (Hippoglossus hippoglossus), Aquacult., 2004, vol. 230, pp. 313–322. https://doi.org/10.1016/S0044-8486(03)00406-X

  42. Ferraris, R.P., Dietary and developmental regulation of intestinal sugar transport, Biochem. J., 2001, vol. 360, pp. 265–276.

  43. Bachelor, D.J, Al-Rammahi, M., Moran, A.W., Brand, J.G., Li, X., Haskins, M., German, A.J., and Shirazi-Beechey, S.P., Sodium/glucose cotransporter-1, sweet receptor, and disaccaridase expression in the intestine of the domestic dog and cat: two species of different dietary habit, Amer. J. Physiol., Reg. Integr. Comp. Physiol., 2011, vol. 300, pp. R67–R75. https://doi.org/10.1152/ajpregu.00262.2010.

  44. Gruzdkov, A.A., Gromova, L.V., Grefner, N.M., and Komissarchik, Yu.Y., Kinetics and mechanisms of glucose absorption in the rat small intestine under physiological conditions, Biophys. Chem., 2012, vol. 3, pp. 191–200. https://doi.org/10.4236/jbpc.2012.32021

  45. Stokes, R. and Fromm, P., Clucose absorption and metabolism by the gut of rainbow trout, Comp. Biochem. Physiol., 1964, vol. 13, pp. 53–69.

  46. Golovanova, I.L., Characteristics of carbohydrate transport in different parts of the intestines of bream (Abramis brama) and carp (Cyprinus carpio), J. Ichthyol., 1993, vol. 33, pp. 26–35.

  47. Sala-Rabanal, M., Gallardo, M.A., Sanchez, J., and Planas, J.M., Na-dependent D-glucose transport by intestinal brush border membrane vesicles from gilthead sea bream (Sparus aurata), J. Membr. Biol., 2004, vol. 201, pp. 85–96.

  48. Hall, J.R., Short, C.E., and Driedzic, W.R., Sequence of Atlantic cod (Gadus morhua) GLUT4, GLUT2, and GPDH: developmental stage expression, tissue expression and relationship to starvation-induced changes in blood glucose, J. Exp. Biol., 2006, vol. 209, pp. 4490–4502.

  49. Cartier, M., Buclon, M., and Robinson, T.W.L., Preliminary studies on the characteristics of phenylalanine and methyl-glucoside transport in the tench intestine in vitro, Comp. Biochem. Physiol. A, 1979, vol. 62, pp. 363–370.

  50. Sastry, K.V., Garg, V.K., and Agrawal, V.P., Effect of inhibitors on Na+-dependent D-glucose transport in the small intestine of two teleost fishes, Indian J. Exp. Biol., 1977, vol. 15, pp. 661–662.

  51. Buddington, R.K., Chen, J., and Diamond, J.M., Genetic and phenotypic adaptation of intestinal nutrient transport to diet in fish, J. Physiol., 1987, vol. 393, pp. 261–281.

  52. Ahearn, G.A., Behnke, R.D., Zonno, V., and Storelli, C., Kinetic heterogeneity of Na-D-glucose cotransport in teleost gastrointestinal tract, Am. J. Physiol., 1992, vol. 263, pp. R1018–R1023.

  53. Hall, J.R., Short, C.E., and Driedzic, W.R., Sequence of Atlantic cod (Gadus morhua) GLUT4, GLUT2, and GPDH: developmental stage expression, tissue expression and relationship to starvation-induced changes in blood glucose, J. Exp. Biol., 2006, vol. 209, pp. 4490–4502.

  54. Deng, D., Yan, X., Zhao, W., Qin, C., Yang, G., and Nie, G., Glucose transporter 2 in common carp (Cyprinus carpio L.): molecular cloning, tissue expression, and the responsiveness to glucose, insulin, and glucagon, Fish Physiol. Biochem., 2020. https://doi.org/10.1007/s10695-020-00782-z

  55. Zhao, W., Qin, C., Yang, G., Zhao, W., Qin, C., Yang, G., Yan, X., Meng, X., Yang, L., Lu, R., Deng, D., Niu, M., and Nie, G., Expression of glut2 in response to glucose load, insulin and glucagon in grass carp (Ctenophcuyngodon idellus), Comp. Biochem. Physiol., Pt. B, 2020, vol. 239, 110351. https://doi.org/10.1016/j.cbpb.2019.110351

  56. Tocher, D.R., Metabolism and functions of lipids and fatty acids in teleost fish, Rev. Fish. Sci., 2003, vol. 11, pp. 107–184.

  57. Kapoor, B.C., Smit, H., and Verighina, I.A., The alimentary canal and digestion in teleosts, Adv. Marine Biol., New York, 1975, vol. 13, pp. 109–239.

  58. Caballero, M.J., Izquierdo, M.S., Kjørsvik, E., Montero, D., Socorro, J., Fernández, A.J., and Rosenlund, G., Morphological aspects of intestinal cells from gilthead seabream (Sparus aurata) fed diets containing different lipid sources, Aquacult., 2003, vol. 225, pp. 325–340.

  59. Ezeasor, D.N. and Stokoe, W.M., Light and electron microscopic studies on the absorptive cells of the intestine caeca and rectum of the adult rainbow trout, Saimo gairdneri Rich, J. Fish Biol., 1981, vol. 18(5), pp. 527–544.

  60. Titus, E., Short-chain fatty acid transport in intestinal brush border membrane vesicles of the african tilapia Oreochromis mossambicus, Pacif. Sci., 1988, vol. 42(1), pp. 134–135.

  61. Sire, M.-F., Lutton, C., and Vernier, J.-M., New views on intestinal absorption of lipids in teleostean fishes: an ultrastructural and biochemical study in the rainbow trout, J. Lipid Res., 1981, vol. 22, pp. 81–94.

  62. Ostos Garrido, M.V., Nunez Torres, M.V., and Abaurrea Equisoaian, M.A., Lipid absorption by enterocytes of the rainbow trout Onchorhyncus mykiss. Diet-induced changes in the endomembranous system, Aquacult., 1993, vol. 110, pp. 156–174.

  63. Hernandez-Blazquez, F.J., Guerra, R.R., Kfoury, J.R., Bombonato, P.P., Cogliati, B., and da Silva, J.R.M.C., Fat absorptive processes in the intestine of the Antarctic fish Notothenia coriiceps (Richardson, 1844), Polar Biol., 2006, vol. 29, pp. 831–836.

  64. Olsen, R.E., Myklebust, R., Kaino, T., and Ringø, E., Lipid digestibility and ultrastructural changes in the enterocytes of Arctic char (Salvelinus alpinus L.) fed linseed oil and soybean lecithin, Fish Physiol. Biochem., 1999, vol. 21, pp. 35–44.

  65. Røsjø, C., Nordrum, S., Olli, J.J., Krogdahl, Å., Ruyter, B., and Holm, H., Lipid digestibility and metabolism in Atlantic salmon (Salmo salar) fed medium-chain triglycerides, Aquacult., 2000, vol. 190, pp. 65–76.

  66. Denstadli, V., Vegusdal, A., Krogdahl, Å., Bakke-McKellep, A.M., Berge, G.M., Holm, H., Hillestad, M., and Ruyter, B., Lipid absorption in different segments of the gastrointestinal tract of Atlantic salmon (Salmo salar L.), Aquacul., 2004, vol. 240, pp. 385–398.

  67. Oxley, A., Jutfel, F., Sundell, K., and Olsen, R.E., Sn-2-monoacylglycerol, not glycerol, is preferentially utilised for triacylglycerol and phosphatidylcholine biosynthesis in Atlantic salmon (Salmo salar L.) intestine, Comp. Biochem. Physiol. B, 2007, vol. 146, pp. 115–123.

  68. André, M., Ando, S., Ballagny, C., Durlait, M., Poupard, G., Briançon, C., and Babin, P.J., Intestinal fatty acid binding protein gene expression reveals the cephalocaudal patterning during zebrafish gut morphogenesis, Inter. J. Dev. Biol., 2000, vol. 44, pp. 249–252.

  69. Esteves, A., Knoll-Gellida, A., Canclini, L., Silvarrey, M.C., André, M., and Babin, P.J., Fatty acid-binding proteins have the potential to channel dietary fatty acids into enterocyte nuclei, J. Lipid Res., 2016, vol. 57(2), pp. 219–332. https://doi.org/10.1194/jlr.M062232.

  70. Shephard, K. L., Functions for fish mucus, Rev. Fish Biol. Fisher., 1994, vol. 4, pp. 401–429.

  71. Krogdahl, Å., Nordrum, S., Sørensen, M., Brudeseth, L., and Røsjø, C., Effects of diet composition on apparent nutrient absorption along the intestinal tract and of subsequent fasting on mucosal disaccharidase activities and plasma nutrient concentration in Atlantic salmon Salmo salar L., Aquacult. Nutr., 1999, vol. 5, pp. 121–133.

  72. Nordrum, S., Krogdahl, Å., Røsjø, C., Olli, J.J., and Holm, H., Effects of methionine, cysteine and medium chain tryglycerides on nutrient digestibility, absorption of amino acids along the intestinal tract and nutrient retention in Atlantic salmon (Salmo salar L.) under pair-feeding regime, Aquacult., 2000, vol. 186, pp. 341–360.

  73. Jutfelt, F., Olsen, R.E., Bjőrnsson, B.T., and Sundell, K., Parr–smolt transformation and dietary vegetable lipids affect intestinal nutrient uptake, barrier function and plasma cortisol levels in Atlantic salmon, Aquacult., 2007, vol. 273, pp. 298–311.

  74. Buddington, R.K. and Doroshov, S.I., Development of digestive secretions in white sturgeon juveniles (Acipenser transmontanus), Comp. Biochem. Physiol. A, 1986, vol. 83(2), pp. 233–238.

  75. Verri, T., Rimoldi, S., Bernardini, G., and Saroglia, M., Impact of feed availability on PEPT1 mRNA expression levels in sea bass (Dicentrarchus labrax), Aquacult., 2009, vol. 294, pp. 288–299. https://doi.org/10.1016/j.aquaculture.2009.06.014

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Russian Text © The Author(s), 2021, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2021, Vol. 57, No. 2, pp. 94–102https://doi.org/10.31857/S0044452921020030.

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Kuz’mina, V.V. Specific Features of Nutrient Transport in the Digestive Tract of Fish. J Evol Biochem Phys 57, 175–184 (2021). https://doi.org/10.1134/S0022093021020010

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