Abstract
This study aimed to determine the level of some brush border and pancreatic digestive enzymes through different stages of feeding and food shifts from hatching to 540 degree days post-hatching (ddph) in Stellate sturgeon (Acipenser stellatus). The evaluated brush border enzymes are alkaline phosphatase, aminopeptidase N, and leucine alanine peptidase, and the pancreatic ones are α-amylase, and bile salt-activated lipase. The results revealed that all these either brush border or pancreatic were present at hatching. Intercellular brush border enzymes including alkaline phosphatase and aminopeptidase N reached their highest levels at 234 and 288 ddph (2.93 ± 0.12 and 3.64 ± 0.14 U mg protein−1 respectively) which were significantly different from hatching. Despite showing some fluctuations to the end, they remained high which can be suitable proof of the initiation of digestive activity in the intestine lumen. The highest specific activity of leucine alanine peptidase was observed at 234 ddph (0.15 ± 0.006 U mg protein−1)and then started to decrease significantly to the end which indicates the transformation of digestion into intercellular form. Pancreatic enzymes including α-amylase and bile salt-activated lipase were high at hatching (7.39 ± 2 and 7.26 ± 0.8 U mg protein−1) showing some fluctuations to the end. This high level at hatching can emphasize the necessity of the ability to consume the yolk sac composition right at hatching. The fluctuations at weaning stages can be due to the carbohydrate and lipid composition of diets.
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References
Asgari R, Rafiee G, Eagderi S, Noori F, Agh N, Poorbagher H, Gisbert E (2013) Ontogeny of the digestive enzyme activities in hatchery produced Beluga (Huso huso). Aquaculture 416:33–40. https://doi.org/10.1016/j.aquaculture.2013.08.014
Babaei SS, Abedian Kenari A, Nazari R, Gisbert E (2011) Developmental changes of digestive enzymes in Persian sturgeon (Acipenser persicus) during larval ontogeny. Aquaculture 318:138–144. https://doi.org/10.1016/j.aquaculture.2011.04.032
Baglole C, Goff G, Wright GM (1998) Distribution and ontogeny of digestive enzymes in larval yellowtail and winter flounder. J Fish Biol 53:767–784. https://doi.org/10.1111/j.1095-8649.1998.tb01831.x
Bessey O, Lowry O, Brock M (1946) A method for the rapid determination of alkaline Organic fluoro-compounds in human plasma phosphatase with five cubic millimetres of serum. Prevalence and characterisation. J Biol Chem 164:321–329
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Buddington R (1985) Digestive secretions of lake sturgeon, Acipenser fulvescens, during early development. J Fish Biol 26:715–723. https://doi.org/10.1111/j.1095-8649.1985.tb04311.x
Buddington RK, Christofferson JP (1985) Digestive and feeding characteristics of the chondrosteans. Environ Biol Fishes 14:31–41. https://doi.org/10.1007/BF00001574
Buddington R (2002). Intestinal absorption of nutrients during early development of vertebrates: patterns of appearance and change. In Biology of growing animals, pp 539–562: Elsevier
Cahu C, Infante JZ (2001) Substitution of live food by formulated diets in marine fish larvae. Aquaculture 200:161–180. https://doi.org/10.1016/S0044-8486(01)00699-8
Castro-Ruiz D, Mozanzadeh MT, Fernández-Méndez C, Andree KB, García-Dávila C, Cahu C, Gisbert E, Darias MJ (2019) Ontogeny of the digestive enzyme activity of the Amazonian pimelodid catfish Pseudoplatystoma punctifer (Castelnau, 1855). Aquaculture 504:210–218. https://doi.org/10.1016/j.aquaculture.2019.01.059
Cominassi L, Moyano M, Claireaux G, Howald S, Mark FC, Zambonino-Infante J-L, Peck MA (2020) Food availability modulates the combined effects of ocean acidification and warming on fish growth. Sci Rep 10:1–12. https://doi.org/10.1038/s41598-020-58846-2
Gawlicka A, Teh S, Hung S, Hinton D, De La Noüe J (1995) Histological and histochemical changes in the digestive tract of white sturgeon larvae during ontogeny. Fish Physiol Biochem 14:357–371
Ghasemi N, Imani A, Noori F, Shahrooz R (2020) Ontogeny of digestive tract of stellate sturgeon (Acipenser stellatus) from hatching to juvenile stage: Digestive enzymes activity, stomach and proximal intestine. Aquaculture 519:734–751. https://doi.org/10.1016/j.aquaculture.2019.734751
Gisbert E, Doroshov SI (2006) Allometric growth in green sturgeon larvae. J Appl Ichthyol 22:202–207
Gisbert E, Sarasquete C (2000) Histochemical identification of the black-brown pigment granules found in the alimentary canal of Siberian sturgeon (Acipenser baeri) during the lecitotrophic stage. Fish Physiol Biochem 22:349–354. https://doi.org/10.1023/A:1007895207177
Gisbert E, Rodriguez A, Castelló-Orvay F, Williot P (1998) A histological study of the development of the digestive tract of Siberian sturgeon (Acipenser baeri) during early ontogeny. Aquaculture 167:195–209. https://doi.org/10.1016/S0044-8486(98)00312-3
Gisbert E, Sarasquete M, Williot P, Castelló-Orvay F (1999) Histochemistry of the development of the digestive system of Siberian sturgeon during early ontogeny. J Fish Biol 55:596–616. https://doi.org/10.1111/j.1095-8649.1999.tb00702.x
Gisbert E, Asgari R, Rafiee G, Agh N, Eagderi S, Eshaghzadeh H, Alcaraz C (2014a) Early development and allometric growth patterns of beluga Huso huso (Linnaeus, 1758). J Appl Ichthyol 30:1264–1272. https://doi.org/10.1111/jai.12617
Gisbert E, Nolasco H, Solovyev M (2018) Towards the standardization of brush border purification and intestinal alkaline phosphatase quantification in fish with notes on other digestive enzymes. Aquaculture 487:102–108. https://doi.org/10.1016/j.aquaculture.2018.01.004
Gisbert E, Moreira, C, Castro-Ruiz, D, Öztürk, S, Fernández, C, Gilles, S, Nuñez, J, Duponchelle, F, Tello, S, Renno, J-F (2014b) Histological development of the digestive system of the Amazonian pimelodid catfish Pseudoplatystoma punctifer. Animal 8: 1765–1776. https://doi.org/10.1017/S1751731114001359
Golchinfar F, Zamani A, Hajimoradloo A, Madani R (2011) Assessment of digestive enzymes activity during the fry development of Rainbow Trout, Oncorhynchus mykiss: from hatching to primary stages after yolk sac absorption. Iran J Fish Sci 10:403–414
Green BS, McCormick MI (2001) Ontogeny of the digestive and feeding systems in the anemonefish Amphiprion melanopus. Environ Biol Fishes 61:73–83. https://doi.org/10.1023/A:1011044919990
Havelka M, Kašpar, V, Hulák, M, Flajšhans, M (2011) Sturgeon genetics and cytogenetics: a review related to ploidy levels and interspecific hybridization. Folia Zool 60: 93–103. https://doi.org/10.25225/fozo.v60.i2.a3.2011
Hoehne-Reitan K, Kjørsvik E (2004) Functional development of liver and pancreas in teleost fish. The development of form and function in fishes and the question of larval adaptation. Am Fish Soc 12:9–37
Hoseini SM, Hosseini SA, Nodeh AJ (2011) Serum biochemical characteristics of Beluga, Huso huso (L.), in response to blood sampling after clove powder solution exposure. Fish Physiol Biochem 37:567–572. https://doi.org/10.1007/s10695-010-9458-8
Iijima N, Tanaka S, Ota Y (1998) Purification and characterization of bile salt-activated lipase from the hepatopancreas of red sea bream, Pagrus major. Fish Physiol Biochem 18:59–69. https://doi.org/10.1023/A:1007725513389
Kamarudin M, Otoi S, Saad C (2011) Changes in growth, survival and digestive enzyme activities of Asian redtail catfish, Mystus nemurus, larvae fed on different diets. Afr J Biotechnol 10:4484–4493. https://doi.org/10.5897/AJB09.1895
Lazo J P, Darias, M J, Gisbert, E (2011) Ontogeny of the digestive tract
López-Ramírez G, Cuenca-Soria C, Alvarez-González C, Tovar-Ramírez D, Ortiz-Galindo JL, Perales-García N, Márquez-Couturier G, Arias-Rodríguez L, Indy J, Contreras-Sánchez W (2011) Development of digestive enzymes in larvae of Mayan cichlid Cichlasoma urophthalmus. Fish Physiol Biochem 37:197–208
Maroux S, Louvard D, Barath J (1973) The aminopeptidase from hog intestinal brush border. Biochim Biophys Acta Enzy 321:282–295. https://doi.org/10.1016/0005-2744(73)90083-1
Métais P, Bieth J (1968) Dètermination de l’a-amylase par unemicrotechnique. Ann Biol Clin 26:133–142
Mir IN, Srivastava P, Bhat IA, Dar SA, Sushila N, Varghese T, Muralidhar A, Jain K (2019) Expression and activity of key lipases during the larval development of walking catfish (Clarias magur). J Exp Zool B Mol 332:149–157. https://doi.org/10.1002/jez.b.22861
Morais S, Conceição L, Rønnestad I, Koven W, Cahu C, Infante JZ, Dinis M (2007) Dietary neutral lipid level and source in marine fish larvae: effects on digestive physiology and food intake. Aquaculture 268:106–122. https://doi.org/10.1016/j.aquaculture.2007.04.033
Nazemroaya S, Yazdanparast R, Nematollahi MA, Farahmand H, Mirzadeh Q (2015) Ontogenetic development of digestive enzymes in Sobaity sea bream Sparidentex hasta larvae under culture condition. Aquaculture 448:545–551. https://doi.org/10.1016/j.aquaculture.2015.06.038
Nicholson JA, Kim YS (1975) A one-step l-amino acid oxidase assay for intestinal peptide hydrolase activity. Anal Biochem 63:110–117. https://doi.org/10.1016/0003-2697(75)90194-3
Pradhan PK, Jena J, Mitra G, Sood N, Gisbert E (2013) Ontogeny of the digestive enzymes in butter catfish Ompok bimaculatus (Bloch) larvae. Aquaculture 372:62–69. https://doi.org/10.1016/j.aquaculture.2012.10.024
Rønnestad I, Yúfera M, Ueberschär B, Ribeiro L, Sæle Ø, Boglione C (2013) Feeding behaviour and digestive physiology in larval fish: current knowledge, and gaps and bottlenecks in research. Rev Aquac 5:S59–S98. https://doi.org/10.1111/raq.12010
Sanz A, Llorente J, Furné M, Ostos-Garrido M, Carmona R, Domezain A, Hidalgo M (2011) Digestive enzymes during ontogeny of the sturgeon Acipenser naccarii: intestine and pancreas development. J Appl Ichthyol 27:1139–1146. https://doi.org/10.1111/j.1439-0426.2011.01864.x
Solovyev M, Kashinskaya E, Izvekova G, Gisbert E, Glupov V (2014) Feeding habits and ontogenic changes in digestive enzyme patterns in five freshwater teleosts. J Fish Biol 85:1395–1412. https://doi.org/10.1111/jfb.12489
Tengjaroenkul B, Smith BJ, Smith SA, Chatreewongsin U (2002) Ontogenic development of the intestinal enzymes of cultured Nile tilapia, Oreochromis niloticus L. Aquaculture 211:241–251. https://doi.org/10.1016/S0044-8486(01)00888-2
Uscanga-Martínez A, Perales-García N, Alvarez-González C, Moyano F, Tovar-Ramírez D, Gisbert G, Márquez-Couturier G, Contreras-Sánchez W, Arias-Rodríguez L, Indy J (2011) Changes in digestive enzyme activity during initial ontogeny of bay snook Petenia splendida. Fish Physiol Biochem 37:667–680. https://doi.org/10.1007/s10695-011-9467-2
Vecsei P, Peterson D, Suciu R, Artyukhin E (2007) Threatened fishes of the world, Acipenser stellatus, Pallas, 1771 (Acipenseridae). Environ Biol Fishes 78:211. https://doi.org/10.1007/s10641-006-0005-5
Yúfera M, Moyano, F J, Martínez-Rodríguez, G (2018). The digestive function in developing fish larvae and fry. From molecular gene expression to enzymatic activity. In Emerging issues in fish larvae research, pp. 51–86: Springer
Zambonino-Infante J L, Gisbert, E, Sarasquete, C, Navarro, I, Gutiérrez, J, Cahu, C L (2008). Ontogeny and physiology of the digestive system of marine fish larvae
Acknowledgements
We highly appreciate Shohadaye Kheybar Sturgeon rearing center for their assistance in providing Stellate larvae and some laboratory conditions for this research. Moreover, we would like to thank Mr. Amin Zarrabi for his great assistance and collaboration.
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This research was under the funding support of Isfahan University of Technology and Iran National Science Foundation.
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All authors contributed to the study conception, design, material preparation, data collection, and analysis. The first draft of the manuscript was written by Amir Masoud Moradian and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Moradian, A.M., Paykan Heyrati, F., Noori, F. et al. The Early Ontogeny of Some Pancreatic and Brush Border Enzymes in the Hatchery Produced Stellate Sturgeon, Acipenser stellatus. Iran J Sci (2024). https://doi.org/10.1007/s40995-024-01638-4
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DOI: https://doi.org/10.1007/s40995-024-01638-4