Postprandial In vitro Protease-Specific Activity of Nile Tilapia (Oreochromis niloticus L.) Digestive Organs
DOI:
https://doi.org/10.3923/pjn.2019.125.133Keywords:
Digestive organs, feeding time, fish feed, Oreochromis niloticus L., pH, postprandial and protease-specific activityAbstract
Background and Objective: Protease-specific activity varies postprandially. This study aimed to identify the optimum time after feeding Nile tilapia (Oreochromis niloticus L.) to collect digestive organ samples (stomach, proximal intestine, distal intestine and liver) to obtain maximum protease-specific activity values. Materials and Methods: One hundred Nile tilapia (average weight 55.19±1.78 g/fish) were acclimatized and fed two times per day for 14 days. At the beginning of the experiment, 6 fish were randomly taken from the tank before feeding (0 h) and then 6 fish were also randomly taken after feeding at 1, 3, 6, 12, 18, 24, 36 and 48 h for digestive organ collection. Homogenized organ pH was measured and extracted for a protease-specific activity assay using azocasein as a substrate. Results: The pH values of all organs differed (p<0.05) after feeding and the pH changes were related to chyme movement in these organs. The protease-specific activities of the stomach and proximal intestine were highest at 24 h after feeding (p<0.05) but the protease-specific activities of the distal intestine and liver were not significantly different (p>0.05) between time points. Conclusion: Postprandial digestive organ sample collection was recommended at 24 h to maximize protease-specific activity for further protease characterization.
References
Gupta, M.V. and B.O. Acosta, 2004. A review of global tilapia farming practices. Aquacult. Asia, 9: 7-12.
Ansah, Y., E. Frimpong and E. Hallerman, 2014. Genetically-improved Tilapia strains in Africa: Potential benefits and negative impacts. Sustainability, 6: 3697-3721.
Fitzsimmons, K.M., 2016. Supply and demand in Global Tilapia markets 2015. https://www.researchgate.net/publication/281241348_Global_Tilapia_Market_update_2015.
Hasan, M.R., 2007. Economics of aquaculture feeding practices in selected Asian countries. FAO Fisheries Technical Paper No. 505, pp: 205.
Hasan, M.R., T. Hecht, S.S. De Silva and A.D.J. Tacon, 2007. Study and analysis of feeds and fertilizers for sustainable aquaculture development. FAO Technical Paper 497, FAO, Rome, pp: 512. http://www.fao.org/docrep/011/a1444e/a1444e00.htm.
El-Sayed, A.F.M., 2004. Protein nutrition of farmed tilapia: Searching for unconventional sources. New dimensions farmed tilapia. Proceedings of the 6th International Symposium on Tilapia in Aquaculture, September 12-16, 2004, Manila, Philippines, pp: 364-378.
Abdel-Tawwab, M., M.H. Ahmad, Y.A.E. Khattab and A.M.E. Shalaby, 2010. Effect of dietary protein level, initial body weight and their interaction on the growth, feed utilization and physiological alterations of Nile tilapia, Oreochromis niloticus (L.). Aquaculture, 298: 267-274.
FAO., 2012. Essential nutrients-proteins and amino acids. Publishing Fish. Aquac. Department. http://www.fao.org/docrep/field/003/ab470e/AB470E02.htm.
Mohanta, K.N., S. Subramanian and V.S. Korikanthimath, 2013. Evaluation of different animal protein sources in formulating the diets for blue gourami, Trichogaster trichopterus fingerlings. J. Aquacult. Res. Dev., Vol. 4.
Pereira, R., L.M.P. Valente, I. Sousa-Pinto and P. Rema, 2012. Apparent nutrient digestibility of seaweeds by rainbow trout (Oncorhynchus mykiss) and Nile tilapia (Oreochromis niloticus). Algal Res., 1: 77-82.
Alarcon, F.J., M. Diaz and F.J. Moyano, 1997. Studies on digestive enzymes in fish: Characterization and practical applications. Cah Options Mediterraneennes, 22: 113-121.
Garcia-Carreno, F.L., A.N. del Toro and M. Ezquerra, 1997. Digestive shrimp proteases for evaluation of protein digestibility in vitro. I: Effect of protease inhibitors in protein ingredients. J. Mar. Biotechnol., 5: 36-40.
Caruso, G., M.G. Denaro and L. Genovese, 2009. Digestive enzymes in some teleost species of interest for mediterranean aquaculture. Open Fish Sci. J., 2: 74-86.
Clements, K.D., D. Raubenheimer and J.H. Choat, 2009. Nutritional ecology of marine herbivorous fishes: Ten years on. Funct. Ecol., 23: 79-92.
Klahan, R., N. Areechon, R. Yoonpundh and A. Engkagul, 2009. Characterization and activity of digestive enzymes in different sizes of Nile tilapia (Oreochromis niloticus L.). Kasetsart J. Nat. Sci., 43: 143-153.
Sultana, Z., S. Ahmed, S. Iqball and A.H. Chisty, 2010. Determination of in vitro protein digestibility of different feed ingredients for Nilotica (Oreochromis nilotica). Bangladesh Res. Public. J., 4: 87-94.
Lin, S. and L. Luo, 2011. Effects of different levels of soybean meal inclusion in replacement for fish meal on growth, digestive enzymes and transaminase activities in practical diets for juvenile tilapia, Oreochromis niloticus × O. aureus. Anim. Feed Sci. Technol., 168: 80-87.
Marquez, L., R. Robles, G.A. Morales and F.J. Moyano, 2012. Gut pH as a limiting factor for digestive proteolysis in cultured juveniles of the gilthead sea bream (Sparus aurata). Fish Physiol. Biochem., 38: 859-869.
Martinezâ€Montano, E. and J.P. Lazo, 2012. In vitro protein digestibility of dietary ingredients throughout ontogeny of California halibut, Paralichthys californicus, larvae. J. World Aquacult. Soc., 43: 51-62.
Thongprajukaew, K., U. Kovitvadhi, S. Kovitvadhi, A. Engkagul and K. Rungruangsak-Torrissen, 2013. Evaluation of growth performance and nutritional quality of diets using digestive enzyme markers and in vitro digestibility in Siamese fighting fish (Betta splendens Regan, 1910). Afr. J. Biotechnol., 12: 1689-1702.
Yasumaru, F. and D. Lemos, 2014. Species specific in vitro protein digestion (pH-stat) for fish: Method development and application for juvenile rainbow trout (Oncorhynchus mykiss), cobia (Rachycentron canadum) and Nile tilapia (Oreochromis niloticus). Aquaculture, 426: 74-84.
Jan, M. and I. Ahmed, 2016. Assessment of fecundity, gonadosomatic index and hepatosomatic index of snow trout, Schizothorax plagiostomus in river Lidder, from Kashmir Himalaya, India. Int. J. Fish. Aquat. Stud., 4: 370-375.
El-Sayed, A.F., I. Nmartinez and F.J. Moyano, 2000. Assessment of the effect of plant inhibitors on digestive proteases of Nile tilapia using in vitro assays. Aquacult. Int., 8: 403-415.
Pujante, I.M., M. Diaz-Lopez, J.M. Mancera and F.J. Moyano, 2017. Characterization of digestive enzymes protease and α-amylase activities in the thick-lipped grey mullet (Chelon labrosus, Risso 1827). Aquacult. Res., 48: 367-376.
Chong, A.S.C., R. Hashim, L. Chow-Yang and A.B. Ali, 2002. Partial characterization and activities of proteases from the digestive tract of discus fish (Symphysodon aequifasciata). Aquaculture, 203: 321-333.
Areekijseree, M., A. Engkagul, U. Kovitvadhi, A. Thongpan, M. Mingmuang, P. Pakkong and K. Rungruangsak-Torrissen, 2004. Temperature and pH characteristics of amylase and proteinase of adult freshwater pearl mussel, Hyriopsis (Hyriopsis) bialatus Simpson 1900. Aquaculture, 234: 575-587.
Lemos, D., A.N. Del Toro, J.H. Cordova-Murueta and F. Garcia-Carreno, 2004. Testing feeds and feed ingredients for juvenile pink shrimp Farfantepenaeus paulensis: In vitro determination of protein digestibility and proteinase inhibition. Aquaculture, 239: 307-321.
Natalia, Y., R. Hashim, A. Ali and A. Chong, 2004. Characterization of digestive enzymes in a carnivorous ornamental fish, the Asian bony tongue Scleropages formosus (Osteoglossidae). Aquaculture, 233: 305-320.
Rungruangsak-Torrissen, K., R. Moss, L.H. Andresen, A. Berg and R. Waagbo, 2006. Different expressions of trypsin and chymotrypsin in relation to growth in Atlantic salmon (Salmo salar L.). Fish Physiol. Biochem., 32: 7-23.
Infante, J.L.Z. and C.L. Cahu, 2007. Dietary modulation of some digestive enzymes and Metabolic processes in developing marine fish: Applications to diet formulation. Aquaculture, 268: 98-105.
Ali, H., M.M. Haque, M.M.R. Chowdhury and M.I. Shariful, 2009. In vitro protein digestibility of different feed ingredients in Thai koi (Anabas testudineus). J. Bangladesh Agric. Univ., 7: 205-210.
De Silva, S.S. and T.A. Anderson, 1995. Fish Nutrition in Aquaculture. Chapman and Hall, London, UK., ISBN-13: 9780412550300, Pages: 319.
Britz, P.J., T. Hecht and J. Knauer, 1996. Gastric evacuation time and digestive enzyme activity in abalone Haliotis midae fed a formulated diet. S. Afr. J. Mar. Sci., 17: 297-303.
Deguara, S., K. Jauncey and C. Agius, 2003. Enzyme activities and pH variations in the digestive tract of gilthead sea bream. J. Fish Biol., 62: 1033-1043.
Montoya, A., J.F. Lopez-Olmeda, M. Yufera, M.J. Sanchez-Muros and F.J. Sanchez-Vazquez, 2010. Feeding time synchronises daily rhythms of behaviour and digestive physiology in Gilthead seabream (Sparus aurata). Aquaculture, 306: 315-321.
Nikolopoulou, D., K.A. Moutou, E. Fountoulaki, B. Venou, S. Adamidou and M.N. Alexis, 2011. Patterns of gastric evacuation, digesta characteristics and pH changes along the gastrointestinal tract of gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.). Compa. Biochem. Physiol. Part A: Mol. Integr. Physiol., 158: 406-414.
Santos, J.F., P.F. Castro, A.L.G. Leal, A.C.V. de Freitas Junior, D. Lemos, L.B. Carvalho Jr. and R.S. Bezerra, 2013. Digestive enzyme activity in juvenile Nile tilapia (Oreochromis niloticus, L.) submitted to different dietary levels of shrimp protein hydrolysate. Aquacult. Int., 21: 563-577.
Hlophe, S.N., N.A.G. Moyo and I. Ncube, 2014. Postprandial changes in pH and enzyme activity from the stomach and intestines of Tilapia rendalli (Boulenger, 1897), Oreochromis mossambicus (Peters, 1852) and Clarias gariepinus (Burchell, 1822). J. Applied Ichthyol., 30: 35-41.
Kuzmina, V.V., G.V. Zolotareva and V.A. Sheptitskiy, 2014. Effect of pH on the activity of proteinases in intestinal mucosa, chyme and microbiota of fish from the Cuciurgan reservoir. J. Ichthyol., 54: 591-597.
Uscanga, A., F.J. Moyano and C.A. Alvarez, 2010. Assessment of enzymatic efficiency on protein digestion in the tilapia Oreochromis niloticus. Fish Physiol. Biochem., 36: 1079-1085.
Takagi, Y., 2001. Effects of starvation and subsequent refeeding on formation and resorption of acellular bone in tilapia, Oreochromis niloticus. Zool. Sci., 18: 623-629.
Drew, R.E., K.J. Rodnick, M. Settles, J. Wacyk and E. Churchill et al., 2008. Effect of starvation on transcriptomes of brain and liver in adult female zebrafish (Danio rerio). Physiol. Genomics, 35: 283-295.
Sanchez-Muros, M.J., L. Garcia-Rejon, L. Garcia-Salguero, M. de la Higuera and J.A. Lupianez, 1998. Long-term nutritional effects on the primary liver and kidney metabolism in rainbow trout. Adaptive response to starvation and a high-protein, carbohydrate-free diet on glutamate dehydrogenase and alanine aminotransferase kinetics. Int. J. Biochem. Cell Biol., 30: 55-63.
Sakamoto, S., M. Furuichi and Y. Yone, 1978. Effect of starvation on organ weight and chemical component of red sea bream. J. Fac. Agric. Kyushu Univ., 23: 71-77.
Ashwini, L., S. Benakappa, H.N. Anjanayappa and L. Akshay, 2016. Observation on the gonado-somatic index-GSI and hepato-somatic index-HSI of Decapterus russelli Mangaluru coast. Int. J. Eng. Sci. Comput., 6: 7396-7399.
Getachew, T., 1989. Stomach pH, feeding rhythm and ingestion rate in Oreochromis niloticus L. (Pisces: Cichlidae) in Lake Awasa, Ethiopia. Hydrobiologia, 174: 43-48.
Bergman, A.N., P. Laurent, G. Otiang'a-Owiti, H.L. Bergman, P.J. Walsh, P. Wilson and C.M. Wood, 2003. Physiological adaptations of the gut in the Lake Magadi tilapia, Alcolapia graham, an alkaline-and saline-adapted teleost fish. Compa. Biochem. Physiol. Part A: Mol. Integr. Physiol., 136: 701-715.
Papastamatiou, Y.P., S.J. Purkis and K.N. Holland, 2007. The response of gastric pH and motility to fasting and feeding in free swimming blacktip reef sharks, Carcharhinus melanopterus. J. Exp. Mar. Biol. Ecol., 345: 129-140.
Bucking, C. and C.M. Wood, 2009. The effect of postprandial changes in pH along the gastrointestinal tract on the distribution of ions between the solid and fluid phases of chyme in rainbow trout. Aquacult. Nutr., 15: 282-296.
Teferi, Y., D. Admassu and S. Mengistou, 2000. The food and feeding habit of Oreochromis niloticus L. (Pisces: Cichlidae) in lake Chamo, Ethiopia. Ethiop. J. Sci., 23: 1-12.
Alemayehu, N. and G. Abebe, 2004. Food habits and diel feeding rhythm of introduced fish, T. zillii gervais, 1948 (Pisces: Cichlidae) in Lake Zwai, Ethiopia. Ethiop. J. Sci., 27: 9-16.
Elbal, M.T. and B. Agulleiro, 1986. A histochemical and ultrastructural study of the gut of Sparus auratus (Teleostei). J. Submicrosc. Cytol., 18: 335-347.
Simpson, B.K., 2000. Digestive Proteinases from Marine Animals. In: Seafood Enzyme Utilization and Influence on Postharvest, Seafood Quality (Food Science and Technology), Haard, N.F. and B.K. Simpson (Eds.)., 1st Edn., CRC Press, New York, pp: 191-214.
Zhao, J., Y. Liu, J. Jiang, P. Wu and G. Chen et al., 2012. Effects of dietary isoleucine on growth, the digestion and absorption capacity and gene expression in hepatopancreas and intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Aquaculture, 368: 117-128.
El-Beltagy, A.E., T.A. El-Adawy, E.H. Rahma and A.A. El-Bedawey, 2004. Purification and characterization of an acidic protease from the viscera of bolti fish (Tilapia nilotica). Food Chem., 86: 33-39.
Jun-Sheng, L., L. Jian-Lin and W. Ting-Ting, 2006. Ontogeny of protease, amylase and lipase in the alimentary tract of hybrid juvenile tilapia (Oreochromis niloticus × Oreochromis aureus). Fish Physiol. Biochem., 23: 295-303.
Alarcon, F.J., M. Diaz, F.J. Moyano and E. Abellan, 1998. Characterization and functional properties of digestive proteases in two sparids; gilthead seabream (Sparus aurata) and common dentex (Dentex dentex). Fish Physiol. Biochem., 19: 257-267.
Bezerra, R.D.S., J.F.D. Santos, M.A.D.S. Lino, V.L.A. Vieira and L.B. Carvalho Jr., 2000. Characterization of stomach and pyloric caeca proteinases of tambaqui (Colossoma macropomum). J. Food Biochem., 24: 189-199.
Vera, L.M., N. De Pedro, E. Gomez-Milan, M.J. Delgado, M.J. Sanchez-Muros, J.A. Madrid and F.J. Sanchez-Vazquez, 2007. Feeding entrainment of locomotor activity rhythms, digestive enzymes and neuroendocrine factors in goldfish. Physiol. Behav., 90: 518-524.
Fagbenro, O., O. Adedire, O. Fateru, I. Oluwabukola and O. Ogunlana et al., 2005. Digestive enzyme assays in the gut of Oreochromis niloticus Linnaeus 1757, Parachanna (Channa) obscura Gunther 1861 and Gymnarchus niloticus Cuvier 1829. Anim. Res. Int., 2: 292-296.
Abolfathi, M., A. Hajimoradloo, R. Ghorbani and A. Zamani, 2012. Effect of starvation and refeeding on digestive enzyme activities in juvenile roach, Rutilus rutilus caspicus. Compa. Biochem. Physiol. Part A: Mol. Integr. Physiol., 161: 166-173.
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