Comparative assessment of digestive enzyme activities of five fish species from the southwestern Atlantic Ocean
DOI:
https://doi.org/10.47193/mafis.3842025011009Keywords:
Digestive enzymes, marine fish, Argentine SeaAbstract
Due to the scarcity of data cited in the literature, digestive enzyme profiles of fish species from the southwestern Atlantic Ocean are of particular interest. In the present study, the viscera yield and digestive enzymes (acid and alkaline proteinase, lipase and amylase) of the stripped weakfish Cynoscion guatucupa, Brazilian codling Urophycis brasiliensis, Patagonian flounder Paralichthys patagonicus, southern eagle ray Myliobatis goodei and smallnose fanskate Sympterygia bonapartii were determined. All species exhibited high proteolytic activity (acid: 0.44-11.0 UE mg protein-1 and alkaline: 0.11-2.32 UE mg protein-1) as well as moderate lipase (0.07-0.76 UE mg protein-1) and amylase activity (0.03-0.24 UE mg protein-1). Teleost fish exhibited higher enzyme activities than cartilaginous fish, with U. brasiliensis exhibiting the highest activities (proteinases, amylases, and lipases). High-activity enzymes from cold-temperate-adapted organisms, mainly from U. brasiliensis and C. guatucupa, may be the source of marine biotechnological bioactive compounds that are beneficial for biotechnological processes.
Downloads
References
Acuña Plavan A, Verocai JE. 2001. Importancia de la pesquería artesanal y biología de la brótola, Urophycis brasiliensis (Kaup, 1858) (Phycidae, Gadiformes) en la costa uruguaya. Investig Mar. 29 (1): 47-58. DOI: https://doi.org/10.4067/S0717-71782001000100005
Acuña Plavan A, Sellanes J, Rodríguez L, Burone L. 2007. Feeding ecology of Urophycis brasiliensis on the Uruguayan coast of the Río de la Plata estuary. J Appl Ichthyol. 23 (3): 231-239. DOI: https://doi.org/10.1111/j.1439-0426.2007.00855.x
Agrawal VP, Sastry KV, Kaushab SK. 1975. Digestive enzymes of three teleost fishes. Acta Physiol Acad Sci Hung. 46 (2): 93-98.
Anson ML. 1938. The estimation of pepsin, trypsin, papain and cathepsin with hemoglobin. J Gen Physiol. 22 (1): 79-89. DOI: https://doi.org/10.1085/jgp.22.1.79
Arne OSS, Hanna-Kirsti SL, Vibeke O, Nils Peder W 2000. Cold adapted enzymes. Biotechnol Annu Rev. 6: 1-57.
Bernfeld P. 1955. Amylases, α and β. In: Colowick SP, Kaplan NO, editors. Methods in enzymology. Academic Press. p. 149-158. DOI: https://doi.org/10.1016/0076-6879(55)01021-5
Bougatef A. 2013. Trypsins from fish processing waste: characteristics and biotechnological applications–comprehensive review. J Clean Prod. 57: 257-265. DOI: https://doi.org/10.1016/j.jclepro.2013.06.005
Bovcon ND, Góngora ME, Marinao C, González-Zevallos D. 2013. Composición de las capturas y descartes generados en la pesca de merluza común Merluccius hubbsi y langostino patagónico Pleoticus muelleri: un caso de estudio en la flota fresquera de altura del Golfo San Jorge, Chubut, Argentina. Rev Biol Mar Oceanogr. 48 (2): 303-319. DOI: https://doi.org/10.4067/S0718-19572013000200010
Bradford MM. 1976. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72: 248-254. DOI: https://doi.org/10.1006/abio.1976.9999
Caille G, Gonzalez R, Gostonyi A, Ciocco N. 1997. Especies capturadas por las flotas de pesca costera en Patagonia. Programa de biólogos observadores a bordo, 1993-1996. Informes Técnicos del Plan de Manejo Integrado de la Zona Costera Patagónica. 27: 1-21.
Candiotto FB, Freitas-Júnior ACV, Neri RCA, Bezerra RS, Rodrigues RV, Sampaio LA, Tesser MB. 2018. Characterization of digestive enzymes from captive Brazilian flounder Paralichthys orbignyanus. Braz J Biol. 78 (2): 281-288. DOI: https://doi.org/10.1590/1519-6984.06616
Castello JP, Haimovici M, Odebrecht C, Vooren CM. 1997. The continental shelf and slope. Subtropical convergence environments: the coast and sea in the southwestern Atlantic. New York: Springer. 308 p.
Chan AS, Horn MH, Dickson KA, Gawlicka A. 2004. Digestive enzyme activities in carnivores and herbivores: comparisons among four closely related prickleback fishes (Teleostei: Stichaeidae) from a California rocky intertidal habitat. J Fish Biol. 65 (3): 848-858. DOI: https://doi.org/10.1111/j.0022-1112.2004.00495.x
Chaudhuri A, Mukherjee S, Homechaudhuri S. 2012. Diet composition and digestive enzymes activity in carnivorous fishes inhabiting mudflats of Indian Sundarban estuaries. Turk J Fish Aquat Sci. 12 (2): 265-275. DOI: https://doi.org/10.4194/1303-2712-v12_2_11
Cousseau MB. 1993. Las especies del Orden Gadiformes del Atlántico Sudamericano comprendido entre 34° S y 35° S y su relación con las de otras áreas. Frente Marit. 13 (A): 7-108.
Del Valle JC, Michiels MS, Radonic M, López A, Lopez Mañanes AA. 2016. Digestive and metabolic profile at the biochemical level of juvenile flounder Paralichthys orbignyanus (Valenciennes, 1839) (Pleuronectiformes: Paralichthyidae). Pan Am J Aquat Sci. 11 (4): 309-323.
Del Valle JC, Zanazzi AN, Rodriguez YE, Haran NS, Laitano MV, Mallo JC, Fernández-Gimenez AV. 2022. Morphological changes, peptidase activity, and effects of exogenous enzymes in the early ontogeny of Nile tilapia, Oreochromis niloticus. Aquac Int. 30 (4): 1645-1658. DOI: https://doi.org/10.1007/s10499-022-00932-5
Díaz De Astarloa JM. 1994. Las especies del género Paralichthys del Mar Argentino (Pisces, Paralichthyidae). Morfología y sistemática [PhD thesis]. Mar del Plata: Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata. 194 p.
[FAO] Food and Agriculture Organization of the United Nations. 2011. Coastal fisheries of Latin America and the Caribbean. Rome: FAO. 52 p.
Fernández-Gimenez AV. 2019. Properties and some new applications of enzymes from wastes of the shrimp Pleoticus muelleri (Decapoda, Penaeoidea). J Shellfish Res. 38 (3): 635- 642. DOI: https://doi.org/10.2983/035.038.0315
Friedman IS, Behrens LA, Pereira NDLA, Contreras EM, Fernández-Gimenez AV. 2020. Digestive proteases from fish processing wastes: their partial characterization and comparison. 28 July 2020, preprint (version 1). Research Square. [accessed 2024 Dec 12]. DOI: https://doi.org/10.21203/rs.3.rs-45716/v1 DOI: https://doi.org/10.21203/rs.3.rs-45716/v1
Friedman IS, Behrens LA, Pereira NDLA, Contreras EM, Fernández‐Gimenez AV. 2022. Digestive proteinases from the marine fish processing wastes of the South‐West Atlantic Ocean: their partial characterization and comparison. J Fish Biol. 100 (1): 150-160. DOI: https://doi.org/10.1111/jfb.14929
Friedman IS, Fernández-Gimenez AV, Contreras EM. 2023. Kinetic characterization of digestive proteinases extracted from the processing waste of South Atlantic fish. Bioresour Technol Rep. 23: 101563. [accessed 2024 Dec 12]. DOI: https://doi.org/10.1016/j.biteb.2023.101563 DOI: https://doi.org/10.1016/j.biteb.2023.101563
Friedman IS, Fernández-Gimenez AV. 2024. State of knowledge about biotechnological uses of digestive enzymes of marine fishery resources: a worldwide systematic review. Aquac Fish Fish. 9 (5): 812-824. DOI: https://doi.org/10.1016/j.aaf.2023.01.002
García-Carreño FL. 1992. The digestive proteases of langostilla (Pleuroncodes planipes, Decapoda): their partial characterization, and the effect of feed on their composition. Comp Biochem Physiol Part B Biochem Mol Biol. 103 (3): 575-578. DOI: https://doi.org/10.1016/0305-0491(92)90373-Y
González-Félix Ml, De La Reé-Rodríguez C, Perez-Velazquez M. 2020. Partial characterization, quantification and optimum activity of trypsin and lipase from the sciaenids Cynoscion othonopterus, Cynoscion parvipinnis and Cynoscion xanthulus. Arch Biol Sci. 72 (1): 81-93. DOI: https://doi.org/10.2298/ABS191127002G
Hidalgo MC, Urea E, Sanz A. 1999. Comparative study of digestive enzymes in fish with different nutritional habits. Proteolytic and amylase activities. Aquaculture. 170 (3): 267-283. DOI: https://doi.org/10.1016/S0044-8486(98)00413-X
Homaei A, Lavajoo F, Sariri R. 2016. Development of marine biotechnology as a resource for novel proteases and their role in modern biotechnology. Int J Biol Macromol. 88: 542-552. DOI: https://doi.org/10.1016/j.ijbiomac.2016.04.023
Jiao F, Zhang L, Limbu SM, Yin H, Xie Y, Yang Z, Shang L, Kong L, Rong H. 2023. A comparison of digestive strategies for fishes with different feeding habits: digestive enzyme activities, intestinal morphology, and gut microbiota. Ecol Evol. 13 (9): e10499. DOI: https://doi.org/10.1002/ece3.10499
Karasov WH, Douglas AE. 2013. Comparative digestive physiology. Compr Physiol. 3 (2): 741. DOI: https://doi.org/10.1002/j.2040-4603.2013.tb00501.x
Lamas D, Massa A. 2023. Abstract extraction and purification of enzymes from the southern eagle ray (Myliobatis goodei) by-products and their compatibility with detergents: a practical approach towards circular economy. Iran J Fish Sci. 22 (4): 853-870.
Lenchours Pezzano J, Rodriguez YE, Fernández-Gimenez AV, Laitano MV. 2024. Exploring fishery waste potential as antifouling component. Environ Sci Pollution Res. 31 (13): 20159-20171. DOI: https://doi.org/10.1007/s11356-024-32491-y
Liu Y, Li X, Li J, Chen W. 2021. The gut microbiome composition and degradation enzymes activity of black Amur bream (Megalobrama terminalis) in response to breeding migratory behavior. Ecol Evol. 11 (10): 5150-5163. DOI: https://doi.org/10.1002/ece3.7407
Menni RC, Stehmann FW. 2000. Distribution, environment and biology of batoid fishes off Argentina, Uruguay and Brazil. A review. Rev Mus Argent Cienc Nat. 2: 69-109. DOI: https://doi.org/10.22179/REVMACN.2.126
Molina JM, Cazorla AL. 2015. Biology of Myliobatis goodei (Springer, 1939), a widely distributed eagle ray, caught in northern Patagonia. J Sea Res. 95: 106-114. DOI: https://doi.org/10.1016/j.seares.2014.09.006
Nolasco-Soria H, Moyano-López F, Vega-Villasante F, Del Monte- Martínez A, Espinosa-Chaurand L, Gisbert E, Nolasco-Alzaga H. 2018. Lipase and phospholipase activity methods for marine organisms. In: Sandoval G, editor. Lipases and phospholipases. Totowa: Humana Press. p. 139-167. DOI: https://doi.org/10.1007/978-1-4939-8672-9_7
Pereira NDLA, Fangio MF, Rodriguez YE, Bonadero MC, Harán NS, Fernández‐Gimenez AV. 2022. Characterization of liquid protein hydrolysates shrimp industry waste: Analysis of antioxidant and microbiological activity, and shelf life of final product. J Food Process Preserv. 46 (8): e15526. DOI: https://doi.org/10.1111/jfpp.15526
Pereira NDLA, Fernández‐Gimenez AV. 2017. Exogenous enzymes in dairy technology: acidic proteases from processing discards of shrimp Pleoticus muelleri and their use as milk‐clotting enzymes for cheese manufacture. Int J Food Sci Technol. 52 (2): 341-347. DOI: https://doi.org/10.1111/ijfs.13285
Pinheiro J, Bates D, Debroy S, Sarkar D, Heisterkamp S, Van Willigen B, Maintainer R. 2017. Package ‘nlme’. Linear and nonlinear mixed effects models. [accessed 2024 Dec 12]. Version 3.1-134.
Piola AR, Campos EJ, Möller JR OO, Charo M, Martinez C. 2000. Subtropical shelf front of eastern South America. J Geophys Res C Oceans. 105 (3): 6565-6578. DOI: https://doi.org/10.1029/1999JC000300
Rodriguez YE, Laitano MV, Zanazzi AN, Fernández-Gimenez AV, Pereira NDLA, Rivero, G. 2024. Turning fishery waste into aquafeed additives: enhancing shrimp enzymes immobilization in alginate-based particles using electrohydrodynamic atomization. Aquaculture. 587: 740846. DOI: https://doi.org/10.1016/j.aquaculture.2024.740846
Rodriguez YE, Sacristán HJ, Laitano MV, López‐Greco LS, Fernández‐Gimenez AV. 2019. From fish‐processing waste to feed additives for crayfish. J World Aquac Soc. 50 (5): 954-968. DOI: https://doi.org/10.1111/jwas.12585
Sardiña P, Lopez Cazorla AC. 2005. Feeding habits of the juvenile striped weakfish, Cynoscion guatucupa Cuvier 1830, in Bahía Blanca estuary (Argentina): seasonal and ontogenetic changes. Hydrobiologia. 532: 23-38. DOI: https://doi.org/10.1007/s10750-004-8769-0
[SSPyA] Subsecretaría de Pesca y Acuicultura. 2024. Desembarques de capturas marítimas totales, 2024. SSPyA. [accessed 2024 Dec 12]. www.magyp.gob.ar/sitio/areas/pesca_maritima/desembarques/lectura.php?imp=1&tabla=especie_flota_2021.
Stehmann M. 2009. Myliobatis goodei. IUCN 2013. IUCN Red List of Threatened Species (version 2012.2). [accessed 2024 Dec 12]. https://www.iucnredlist.org.
Tian WH, Jun ZP. 2002. Activities of digestive enzyme in different tissues of Paralichthys olivaceus. Oceanol Limnol. 33 (5): 472-476.
Troccoli GH, Milessi AC, Marí N, Figueroa D, De Wysiecki AM. 2021. Trophic ecology of Patagonian flounder Paralichthys patagonicus (Jordan, 1889) in the Argentine-Uruguayan Coastal Ecosystem. Mar Fish Sci. 35 (1): 67-80. DOI: https://doi.org/10.47193/mafis.3512022010109
Vega-Villasante F, Nolasco H, Civera R. 1993. The digestive enzymes of the pacific brown shrimp Penaeus californiensis. I-properties of amylase activity in the digestive tract. Comp Biochem Physiol Part B Biochem Mol Biol. 106 (3): 547-550. DOI: https://doi.org/10.1016/0305-0491(93)90130-W
Versaw WK, Cuppett SL, Winters DD, Williams LE. 1989. An improved colorimetric assay for bacterial lipase in nonfat dry milk. J Food Sci. 54: 1557-1558. DOI: https://doi.org/10.1111/j.1365-2621.1989.tb05159.x
Volkoff H, Rønnestad I. 2020. Effects of temperature on feeding and digestive processes in fish. Temperature. 7 (4): 307-320. DOI: https://doi.org/10.1080/23328940.2020.1765950 DOI: https://doi.org/10.1080/23328940.2020.1765950
Yu L, Yuan Z, Huang X, Gao Z, Liu H. 2024. The difference of the composition and digestive enzymes of gut microbiome in herbivorous blunt snout bream (Megalobrama amblycephala) and carnivorous largemouth bass (Micropterus salmoides). Aquac Fish. 10 (34): 459-468. DOI: https://doi.org/10.1016/j.aaf.2023.12.002 DOI: https://doi.org/10.1016/j.aaf.2024.01.002
Zacarias‐Soto M, Muguet JB, Lazo JP. 2006. Proteolytic activity in California halibut larvae (Paralichthys californicus). J World Aquaculture Soc. 37 (2): 175-185. DOI: https://doi.org/10.1111/j.1749-7345.2006.00024.x
Published
Issue
Section
License
Copyright (c) 2025 María Cecilia Bonadero, María Victoria Laitano, Juana Cristina del Valle, Yamila Eliana Rodriguez, Nair de los Angeles Pereira, Analia Fernández-Gimenez
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Authors of articles published in Marine and Fishery Sciences retain copyright on their articles, except for any third-party images and other materials added by Marine and Fishery Sciences, which are subject to copyright of their respective owners. Authors are therefore free to disseminate and re-publish their articles, subject to any requirements of third-party copyright owners and subject to the original publication being fully cited. Visitors may also download and forward articles subject to the citation requirements. The ability to copy, download, forward or otherwise distribute any materials is always subject to any copyright notices displayed. Copyright notices must be displayed prominently and may not be obliterated, deleted or hidden, totally or partially.
This journal offers authors an Open Access policy. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other legal purpose within the Creative Commons 4.0 license (BY-NC-SA), without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of Open Access.
