Change in Protein Digestion Capacity During Juvenile Fish Ontogeny: Approach on Spotted Rose Snapper (Lutjanus guttatus)
Keywords:
Proteases, enzyme characterization, electrophoresis, in vitro digestibility, Lutjanidae.Abstract
Aquaculture is facing a challenge in order to search new alternative nutritional sources to generate highly
digestible and profitable diets for aquaculture species. In addition, the understanding of changes in digestive
capacity in fish species with aquaculture potential is of relevance importance, as the capacity of assimilation
of different nutrients may change during the juvenile development of the species. Numerous research has
been focused on understanding the changes and adaptations of the development and capacities of the digestive
system during the early ontogeny of fish, minimizing the importance of possible changes during juvenile
ontogeny, as a trigger for the grow-out efficiency increase in fish culture.
Thus, few studies address the digestive changes during juvenile fish ontogeny and their implications in the
ability to assimilate different nutritional sources, considering that there should be no changes during this
stage, which in general represents the period of grow-out until commercial size, prior to their reproductive
stages.
The present work deals with the importance to characterize changes the digestive capacity during grow-out on
the spotted rose snapper (Lutjanus guttatus). Comparative studies of juvenile sizes of the species (20 to 400
grams) have shown existence of changes in the optimum alkaline protease activity, as well as a diversification
and increase in the number of digestive enzymes of the alkaline phase in relation to juvenile ontogeny,
resulting in changes of in vitro hydrolysis degree and total release of amino acids from different protein
sources.
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References
Adler-Nissen J (1986) Enzymatic hydrolysis of food proteins. Elsevier, London, pp 427
Álvarez-González CA, Moyano-López FJ, Civera-Cerecedo R, Carrasco-Chávez V, Ortíz-Galindo JL,
Nolasco-Soria H, Tovar-Ramírez D, Dumas S. (2008) Development of digestive enzyme activity in
larvae of spotted sand bass Paralabrax maculatofasciatus II: Electrophoretic analysis. Fish Physiol
Biochem 34:373–384.
Álvarez-Lajonchère L, Abdo de la Parra MI, Rodríguez-Ibarra LE, Velasco-Blanco G, Puello-Cruz AC,
González-Rodríguez B, Ibarra-Soto A, Ibarra-Castro L. (2012) The scale-up of spotted rose snapper,
Lutjanus guttatus, larval rearing at Mazatlán, Mexico. J World Aquac Soc 43(3):411-42
Allen GR. (1987) Synopsis of the circumtropical fish genus Lutjanus (Lutjanidae). In: Polovina JJ & S
Ralston (eds). Tropical Snappers and Groupers: Biology and Fisheries Management, pp. 33-87.
Westview Press, Boulder, Colorado.
AOAC (Association of Official Analytical Chemists). (2000) Official methods of analysis, 17th edition.
Association of Official Analytical Chemists, Arlington, Virginia, USA.
Bassompierre M, Ostenfeld TH, McLean E, Rungruangsak-Torrissen K. (1998) In vitro protein digestion and
growth of Atlantic salmon with different trypsin isozymes. Aquacult Int 6:47–56
Castillo-Yáñez FJ, Pacheco-Aguilar R, García-Carreño FL, Navarrete-Del Toro MA. (2004) Characterization
of acidic proteolytic enzymes from Monterey sardine (Sardinops sagax caerulea) viscera. Food
Chem 85:343-350
Castillo-Yáñez FJ, Pacheco-Aguilar R, García-Carreño FL, Navarrete-Del Toro MA. (2005) Isolation and
characterization of trypsin from Monterey sardine Sardinops sagax caerulea. Comp Biochem
Physiol B 140:91-98
Castillo-Yáñez FJ, Pacheco-Aguilar R, García-Carreño FL, Navarrete-Del Toro MA, López MF. (2006)
Purification and biochemical characterization of chymotrypsin from the viscera of Monterey sardine
(Sardinops sagax caerulea). Food Chem 99:252-259
Chiu ST, Pan BS (2002) Digestive protease activities of juvenile and adult eel (Anguilla japonica) fed with
floating feed. Aquaculture 205:141-156
Church FC, Swaisgood HE, Porter DH, Catignani G. (1983) Spectrophotometric assay using o-phthaldehyde
for determination of proteolysis in milk proteins. J Dairy Sci 66:1219-1227
Davis BJ (1964) Disc electrophoresis. II. Method and application to human serum proteins. Ann. New York
Acad. Sci. 121:404-427
Díaz-López M, Moyano FJ, Alarcón FJ, García-Carreño FL, Navarrete del Toro MA (1998) Characterization
of fish acid proteases by substrate-gel electrophoresis. Comp Biochem Physiol 121B:369–377
Dimes LE, Haard NF (1994) Estimation of protein digestibility- I. Development of an in vitro method for
estimating protein digestibility in salmonids. Comp Biochem Physiol A 108:349-362
Peña, E. et al., 2017. Change in protein digestion capacity during juvenile fish ontogeny: Approach on spotted rose snapper (Lutjanus guttatus). En: Cruz-Suárez, L.E., Ricque-Marie,
D., Tapia-Salazar, M., Nieto-López, M.G., Villarreal-Cavazos, D. A., Gamboa-Delgado, J., López Acuña, L.M. y Galaviz-Espinoza, M. (Eds), Investigación y Desarrollo en Nutrición
Acuícola Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Nuevo León, México, pp. 408-431. ISBN 978-607-27-0822-8.
Dimes LE, Haard NF, Dong FM, Rasco BA, Forster IP, Fairgrieve WT, Arndt R, Hardy RW, Barrows FT,
Higgs DA. (1994) Estimation of protein digestibility — II. In vitro assay of protein in salmonid feeds.
Comp Biochem Physiol 108A:363–370
El-Mowafi AF, Dorrell H, Bureau DP (2000) Potential of a pH-stat method to estimate apparent digestibility
of protein in salmonids. IX International Symposium on Nutrition and Feeding of Fish, 21-25 May
, Miyazaki, Japan.
Erlanger BF, Kolowsky N, Cohen W (1961) The preparation and properties of two new chromogenic
substrates of trypsin. Arch Biochem Biophys 95:271–278
Ezquerra JM, Garcia-Carreño FL, Civera R, Haard NF (1997) pH-stat method to predict digestibility in vitro
in white shrimp Penaeus vannamei. Aquaculture 157:249-260
Falcón-Hidalgo B, Forrellat-Barrios A, Farnés QC, Hernández KU. (2011) Digestive enzymes of two
freshwater fishes (Limia vittata and Gambusia punctata) with different dietary preferences at three
developmental stages. Comp Biochem Physiol B 158:136–141
Furnè M, García-Gallego M, Hidalgo MC, Morales AE, Domezain A, Domezain J, Sanz A. (2008) Effect of
starvation and refeeding on digestive enzyme activities in sturgeon (Acipenser naccarii) and trout
(Oncorhynchus mykiss). Comp Biochem Physiol A 149:420–425
Galaviz MA, García-Ortega A, Gisbert E, López LM, García-Gasca A. (2012) Expression and activity of
trypsin and pepsin during larval development of the spotted rose snapper Lutjanus guttatus. Comp
Biochem Physiol B 161:9-16
García-Carreño FL, Dimes LE, Haard NF. (1993) Substrate-gel electrophoresis for composition and
molecular weight of proteinases or proteinaceous proteinase inhibitors. Anal Biochem 214:65-69
Guerrero-Zárate R, Álvarez-González CA, Olvera-Novoa MA, Perales-García N, Frías-Quintana CA,
Martínez-García R, Contreras-Sánchez WM. (2014) Partial characterization of digestive proteases in
tropical gar Atractosteus tropicus juveniles. Fish Physiol Biochem. DOI 10.1007/s10695-013-9902-7
Haard NF. (1994) Protein hydrolysis in seafoods In: Shahidi F., J.R. Botta (eds) Seafood chemistry.
Processing Techonology and Quality. Chapman and Hall, New York, pp10-33
Klomklao S, Benjakul S, Visessanguan W. (2004) Comparative studies on proteolytic activity of spleen
extracts from three tuna species commonly used in Thailand. J Food Biochem 28:355-372
Klomklao S, Kishimur H, Yabe M, Benjakul S. (2007) Purification and characterization of two pepsins from
the stomach of pectoral rattail (Coryphaenoides pectoralis). Comp Biochem Physiol B 147(4):682–
Klomklao S. (2008) Digestive proteinases from marine organisms and their applications. Songklanakarin J Sci
Technol 30 (1):37-46
Kolkovski S. (2001) Digestive enzymes in fish larvae and juveniles: implications and applications to
formulated diets. Aquaculture 200:181–201
Kuzʼmina VV. (1996) Influence of age on digestive enzyme activity in some freshwater teleosts. Aquaculture
:25-37
Peña, E. et al., 2017. Change in protein digestion capacity during juvenile fish ontogeny: Approach on spotted rose snapper (Lutjanus guttatus). En: Cruz-Suárez, L.E., Ricque-Marie,
D., Tapia-Salazar, M., Nieto-López, M.G., Villarreal-Cavazos, D. A., Gamboa-Delgado, J., López Acuña, L.M. y Galaviz-Espinoza, M. (Eds), Investigación y Desarrollo en Nutrición
Acuícola Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Nuevo León, México, pp. 408-431. ISBN 978-607-27-0822-8.
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature 227:680–685
Lazo JP, Mendoza R, Holt GL, Aguilera C, Arnold CR. (2007) Characterization of digestive enzymes during
larval development of red drum (Sciaenops ocellatus). Aquaculture. 265:194–205
Lemos D, Tacon AGJ (2011) A rapid low-cost laboratory method for measuring the in vitro protein
digestibility of feed ingredients and feeds for shrimp. Aquacult Asia Pac 7:18-21
Lemos D, Lawrence AL, Siccardi III AJ. (2009) Prediction of apparent protein digestibility of ingredients and
diets by in vitro pH-stat degree of protein hydrolysis with species specific enzymes for juvenile Pacific
white shrimp Litopenaeus vannamei. Aquaculture 295:89-98
Lemos D, Ezquerra JM, García-Carreño FL. (2000) Protein digestion in penaeid shrimps: digestive
proteinases, proteinase inhibitors and feed digestibility. Aquaculture 186:89-105
Matus de la Parra A, Rosas A, Lazo JP, Viana MT. (2007) Partial characterization of the digestive enzymes of
Pacific bluefin tuna Thunnus orientalis under culture conditions. Fish Physiol Biochem 33:223-231
Moguel-Hernández I, Peña R, Nolasco-Soria H, Dumas S, Zavala-Leal I. (2013) Development of digestive
enzyme activity in spotted rose snapper, Lutjanus guttatus (Staeindacher, 1969) larvae. Fish Physiol
Biochem 40(3):839-848
Perera E, Moyano FJ, Rodriguez-Viera L, Cervantes A, Martínez-Rodríguez G, Mancera JM. (2010) In vitro
digestion of protein sources by crude enzyme extracts of the spiny lobster Panulirus argus (Latreille,
hepatopancreas with different trypsin isoenzyme patterns. Aquaculture 310:178-185
Perera E, Rodríguez‑Viera L, Perdomo‑Morales R, Montero‑Alejo V, Moyano FJ, Martínez‑Rodríguez R,
Mancera JM. (2015). Trypsin isozymes in the lobster Panulirus argus (Latreille, 1804): from
molecules to physiology. J Comp Physiol B 185:17-35.
Pérez-Jiménez A, Cardenete G, Morales AE, García-Alcázar A, Abellán E, Hidalgo MC. (2009) Digestive
enzymatic profile of Dentex dentex and response to different dietary formulations. Comp Biochem
Physiol A 154:157–164
Prudence M, Moal J, Boudry P, Daniel JY, Quéré C, Jeffroy F, Mingant C, Ropert M, Bédier E, Van
Wormhoudt A, Samain JF, Huvet A. (2006) An amylase gene polymorphism is associated with growth
differences in the Pacific cupped oyster Crassostrea gigas. Anim Genet 37:348–351.
Rønnestad I, Kamisaka Y, Conceicao LEC, Morais S, Tonheim SK. (2007) Digestive physiology of marine
fish larvae: hormonal control and processing capacity for proteins, peptides and amino acids.
Aquaculture 268:82–97
Rungruangsak-Torrissen K, Pringle GM, Moss R, Houlihan DF. (1998) Effects of varying rearing
temperatures on expression of different trypsin isoenzymes, feed conversion efficiency and growth in
Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 19:247–255
Rust MB. (2002) Nutritional Physiology. En: J. E. Halver y R. W. Hardy (eds.). Fish nutrition. Tercera
edición. Academic press. San Diego, CA, USA. 143-179
Peña, E. et al., 2017. Change in protein digestion capacity during juvenile fish ontogeny: Approach on spotted rose snapper (Lutjanus guttatus). En: Cruz-Suárez, L.E., Ricque-Marie,
D., Tapia-Salazar, M., Nieto-López, M.G., Villarreal-Cavazos, D. A., Gamboa-Delgado, J., López Acuña, L.M. y Galaviz-Espinoza, M. (Eds), Investigación y Desarrollo en Nutrición
Acuícola Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Nuevo León, México, pp. 408-431. ISBN 978-607-27-0822-8.
Salze G, McLean E, Craig SR. (2012) Dietary taurine enhances growth and digestive enzyme activities in
larval cobia. Aquaculture 362–363:44–49
Sarath G, De la Motte RS, Wagner FW. (1989) Protease assay methods In: Beynon R, Bond J (eds)
Proteolytic enzymes: a practical approach. IRL, Oxford, pp25–56
Saunders RM, Conner MA, Booth AN, Bickoff EM, Kohler GO (1972) Measurement of digestibility of
alfalfa concentrates by in vivo and in vitro methods. J Nutr 103:530-535.
Silva-Carrillo Y, Hernández C, Hardy RW, González-Rodríguez B, Castillo-Vargasmachuca S. (2012) The
effect of substituting fish meal with soybean meal on growth, feed efficiency, body composition and
blood chemistry in juvenile spotted rose snapper Lutjanus guttatus (Steindachner, 1869).
Aquaculture 364–365:180–185
Simpson BK. (2000) Digestive proteinases from marine animals. In Seafood Enzymes: Utilization and
Influence on Postharvest Seafood Quality, N.F. Haard and B.K. Simpson, editors. Marcel Dekker,
New York., pp. 531-540.
Tibbetts SM, Milley JE, Ross NW, Verreth JAJ, Lall SP (2011a) In vitro pH-stat protein hydrolysis of feed
ingredients for Atlantic cod, Gadus morhua. 1. Development of the method. Aquaculture 319:398-406
Tibbetts SM, Verreth JAJ, Lall SP. (2011b) In vitro pH-stat protein hydrolysis of feed ingredients for Atlantic
cod, Gadus morhua. 2. In vitro protein digestibility of common and alternative feed ingredients.
Aquaculture 319:407-416
Torrissen KR. (1987) Genetic variation of trypsin-like isozymes correlated to fish size at Atlantic salmon
(Salmo salar). Aquaculture 62:1–10
Torrissen KR (1991) Genetic variation in growth rate of Atlantic salmon with different trypsin-like isozyme
patterns. Aquaculture 93:299–312
Unajak S, Meesawat P, Paemanee A, Areechon N, Engkagul A, Kovitvadhi U, Kovitvadhi S, Rungruangsak-
Torrissen K, Choowongkomon K. (2012) Characterization of thermostable trypsin and determination
of trypsin isozymes from intestine of Nile tilapia (Oreochromis niloticus L). Food Chem
(3):1533-1541
Vázquez RI, Rodríguez J, Abitia LA y Galván F. (2008) Food habits of the yellow snapper Lutjanus
argentiventris (Peters, 1869) (Percoidei: Lutjanidae) in La Paz Bay, Mexico. Rev Biol Mar Oceanogr
(2):295-302
Walter HE. (1984) Proteinases: methods with hemoglobin, casein and azocoll as substrates. In: Bergmeyer
H.U. (eds) Methods of Enzymatic Analysis, Vol. V. Verlag Chemie, Weinheim, pp270–277
Weber K, Osborn M. (1969) The reliability of molecular weight determinations by dodecyl sulfate
polyacrylamide gel electrophoresis. J Biol Chem 244:4406-4412
Yasumaru F, Lemos D. (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 426-427:74-84
Peña, E. et al., 2017. Change in protein digestion capacity during juvenile fish ontogeny: Approach on spotted rose snapper (Lutjanus guttatus). En: Cruz-Suárez, L.E., Ricque-Marie,
D., Tapia-Salazar, M., Nieto-López, M.G., Villarreal-Cavazos, D. A., Gamboa-Delgado, J., López Acuña, L.M. y Galaviz-Espinoza, M. (Eds), Investigación y Desarrollo en Nutrición
Acuícola Universidad Autónoma de Nuevo León, San Nicolás de los Garza, Nuevo León, México, pp. 408-431. ISBN 978-607-27-0822-8