Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Effects of Enzymatic Hydrolysis Conditions on the Antioxidant Activity of Red Tilapia (Oreochromis spp.) Viscera Hydrolysates

Author(s): Cindy T. Sepúlveda* and José E. Zapata

Volume 21, Issue 12, 2020

Page: [1249 - 1258] Pages: 10

DOI: 10.2174/1389201021666200506072526

Price: $65

Abstract

Background: Fish is an essential source of nutrients for human nutrition due to the composition of proteins, vitamins, and minerals, among other nutrients. Enzymatic hydrolysis represents an alternative for the use of by-products of the aquaculture industry.

Objective: We propose to evaluate the effect of stirring speed, temperature, and initial protein concentration on the degree of hydrolysis of proteins and antioxidant activity of red tilapia (Oreochromis spp.) viscera hydrolysates.

Methods: The effect of stirring speed, temperature, and initial protein concentration on the degree of hydrolysis of proteins and antioxidant activity was evaluated using an experimental design that was adjusted to a polynomial equation. The hydrolysate was fractioned to determine the antioxidant activity of the fractions, and functional properties were also measured.

Results: Stirring speed and protein concentration presented a statistically significant effect (p <0.05) on all the response variables. However, the temperature did not present a statistically significant effect on the degree of hydrolysis.

Discussion: The best conditions of hydrolysis were stirring speed of 51.44 rpm, a temperature of 59.15°C, and the protein concentration of 10 g L-1. The solubility of the hydrolysate protein was high at different pH, and the hydrolysate fraction with the highest antioxidant activity has a molecular weight <1 kDa.

Conclusion: The degree of hydrolysis and the biological activity of red tilapia viscera hydrolysates (Oreochromis spp.) are affected by temperature, substrate concentration, and stirring speed. The optimal conditions of hydrolysis allowed to obtain a hydrolysate with antioxidant activity are due to the peptides with low molecular weight.

Keywords: Enzymatic hydrolysis, antioxidant activity, chelating activity, bioactive peptides, response surface methodology, fish hydrolysates, functional properties.

« Previous Next »
Graphical Abstract

[1]
Food and Agriculture Organization of the United Nations. The State of World Fisheries and Aquaculture 2018- Meeting the Sustainable Development Goals; Rome, 2018.
[2]
Josupeit, H. World Market of Tilapia. Globefish Res. Program., 2004, 79, 28.
[3]
Sripokar, P.; Benjakul, S.; Klomklao, S. Antioxidant and functional properties of protein hydrolysates obtained from starry triggerfish muscle using trypsin from Albacore Tuna liver. Biocatal. Agric. Biotechnol., 2019, 17, 447-454.
[http://dx.doi.org/10.1016/j.bcab.2018.12.013]
[4]
Fontoura, R.; Daroit, D.J.; Corrêa, A.P.F.; Moresco, K.S.; Santi, L.; Beys-da-Silva, W.O.; Yates, J.R., III; Moreira, J.C.F.; Brandelli, A. Characterization of a novel antioxidant peptide from feather keratin hydrolysates. N. Biotechnol., 2019, 49, 71-76.
[http://dx.doi.org/10.1016/j.nbt.2018.09.003 ] [PMID: 30223040]
[5]
Robert, M.; Zatylny-Gaudin, C.; Fournier, V.; Corre, E.; Le Corguillé, G.; Bernay, B.; Henry, J. Molecular characterization of peptide fractions of a tilapia (Oreochromis niloticus) by-product hydrolysate and in vitro evaluation of antibacterial activity. Process Biochem., 2015, 50(3), 487-492.
[http://dx.doi.org/10.1016/j.procbio.2014.12.022]
[6]
Benítez, R.; Ibarz, A.; Pagan, J. Hidrolizados de proteína: Procesos y aplicaciones protein hydrolysates: Processes and applications R esumen. Acta Bioquim. Clin. Latinoam., 2008, 42(2), 227-237.
[7]
Opheim, M.; Šližytė, R.; Sterten, H.; Provan, F.; Larssen, E.; Kjos, N.P. Hydrolysis of Atlantic Salmon (Salmo Salar) rest raw materials-effect of raw material and processing on composition, nutritional value, and potential bioactive peptides in the hydrolysates. Process Biochem., 2015, 50(8), 1247-1257.
[http://dx.doi.org/10.1016/j.procbio.2015.04.017]
[8]
Silva, J.F.X.F.X.; Ribeiro, K.; Silva, J.F.X.F.X.; Cahú, T.B.B.; Bezerra, R.S.S. Utilization of tilapia processing waste for the production of fish protein hydrolysate. Anim. Feed Sci. Technol., 2014, 196, 96-106.
[http://dx.doi.org/10.1016/j.anifeedsci.2014.06.010]
[9]
Huang, B. Bin; Lin, H.C.; Chang, Y.W. Analysis of proteins and potential bioactive peptides from Tilapia (Oreochromis Spp.) processing co-products using proteomic techniques coupled with BIOPEP database. J. Funct. Foods, 2015, 19, 629-640.
[http://dx.doi.org/10.1016/j.jff.2015.09.065]
[10]
Chalamaiah, M.; Dinesh Kumar, B.; Hemalatha, R.; Jyothirmayi, T. Fish protein hydrolysates: Proximate composition, amino acid composition, antioxidant activities and applications: A review. Food Chem., 2012, 135(4), 3020-3038.
[http://dx.doi.org/10.1016/j.foodchem.2012.06.100] [PMID: 22980905]
[11]
He, S.; Franco, C.; Zhang, W. Functions, applications and production of protein hydrolysates from Fish Processing Co-Products (FPCP). Food Res. Int., 2013, 50(1), 289-297.
[http://dx.doi.org/10.1016/j.foodres.2012.10.031]
[12]
García-Moreno, P.J.; Batista, I.; Pires, C.; Bandarra, N.M.; Espejo-Carpio, F.J.; Guadix, A.; Guadix, E.M. Antioxidant activity of protein hydrolysates obtained from discarded Mediterranean fish species. Food Res. Int., 2014, 65, 469-476.
[http://dx.doi.org/10.1016/j.foodres.2014.03.061]
[13]
Morales-Medina, R.; Tamm, F.; Guadix, A.M.; Guadix, E.M.; Drusch, S. Functional and antioxidant properties of hydrolysates of sardine (S. pilchardus) and horse mackerel (T. mediterraneus) for the microencapsulation of fish oil by spray-drying. Food Chem., 2016, 194, 1208-1216.
[http://dx.doi.org/10.1016/j.foodchem.2015.08.122] [PMID: 26471673]
[14]
A.O.A.C. Official Methods of Analysis. Asociation of Official Analytical Chemist; Gaithersburg, MD, USA, 2005.
[15]
Baez-Suarez, J.A.; Ospina De Barreneche, N. Zapata Montoya, José, E.Z. Efecto de temperatura, PH, concentración de sustrato y tipo de enzima en la hidrólisis enzimática de vísceras de tilapia Roja (Oreochromis Spp.). Inf. Tecnol., 2016, 27(6), 63-76.
[http://dx.doi.org/10.4067/S0718-07642016000600007]
[16]
Adler-nissen, J. Ensymes in food precessing; Nagodawithana, T; Reed, G., Ed.; , 1993, pp. 159-203.
[http://dx.doi.org/10.1016/B978-0-08-057145-4.50014-1]
[17]
Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med., 1999, 26(9-10), 1231-1237.
[http://dx.doi.org/10.1016/S0891-5849(98)00315-3] [PMID: 10381194]
[18]
Pulido, R.; Bravo, L.; Saura-Calixto, F. Antioxidant activity of dietary polyphenols as determined by a modified ferric reducing/antioxidant power assay. J. Agric. Food Chem., 2000, 48(8), 3396-3402.
[http://dx.doi.org/10.1021/jf9913458 ] [PMID: 10956123]
[19]
Decker, E.A.; Welch, B. Role of ferritin as a lipid oxidation catalyst in muscle food†. J. Agric. Food Chem., 1990, 38(3), 674-677.
[http://dx.doi.org/10.1021/jf00093a019]
[20]
Ou, B.; Hampsch-Woodill, M.; Prior, R.L. Development and validation of an improved oxygen radical absorbance capacity assay using fluorescein as the fluorescent probe. J. Agric. Food Chem., 2001, 49(10), 4619-4626.
[http://dx.doi.org/10.1021/jf010586o ] [PMID: 11599998]
[21]
Peterson, G.L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem., 1977, 83(2), 346-356.
[http://dx.doi.org/10.1016/0003-2697(77)90043-4 ] [PMID: 603028]
[22]
Pacheco-Aguilar, R.; Mazorra-Manzano, M.A.; Ramírez-Suárez, J.C. Functional properties of fish protein hydrolysates from Pacific whiting (Merluccius productus) muscle produced by a commercial protease. Food Chem., 2008, 109(4), 782-789.
[http://dx.doi.org/10.1016/j.foodchem.2008.01.047] [PMID: 26049991]
[23]
Nongonierma, A.B.; Mazzocchi, C.; Paolella, S.; FitzGerald, R.J. Release of dipeptidyl peptidase IV (DPP-IV) inhibitory peptides from Milk Protein Isolate (MPI) during enzymatic hydrolysis. Food Res. Int., 2017, 94, 79-89.
[http://dx.doi.org/10.1016/j.foodres.2017.02.004 ] [PMID: 28290371]
[24]
Guo, Y.; Pan, D.; Tanokura, M. Optimisation of hydrolysis conditions for the production of the Angiotensin-I Converting Enzyme (ACE) inhibitory peptides from whey protein using response surface methodology. Food Chem., 2009, 114(1), 328-333.
[http://dx.doi.org/10.1016/j.foodchem.2008.09.041]
[25]
Feng, L.; Tu, M.; Qiao, M.; Fan, F.; Chen, H.; Song, W.; Du, M. Thrombin inhibitory peptides derived from mytilus edulis proteins: identification, molecular docking and in silico prediction of toxicity. Eur. Food Res. Technol., 2018, 244(2), 207-217.
[http://dx.doi.org/10.1007/s00217-017-2946-7]
[26]
Gómez, L.J.; Zapata, J.E. Efecto Del Nivel de Grasa y velocidad de agitación en la hidrolisis enzimática de vísceras de Tilapia Roja (Orechromis Sp.). Inf. Tecnol., 2017, 28, 47-56.
[http://dx.doi.org/10.4067/S0718-07642017000400007]
[27]
Colombié, S.; Gaunand, A.; Lindet, B. Lysozyme inactivation under mechanical stirring: Effect of physical and molecular interfaces. Enzyme Microb. Technol., 2001, 28(9-10), 820-826.
[http://dx.doi.org/10.1016/S0141-0229(01)00340-4] [PMID: 11397464]
[28]
Elmalimadi, M.B.; Jovanović, J.R.; Stefanović, A.B.; Tanasković, S.J.; Djurović, S.B.; Bugarski, B.M.; Knežević-Jugović, Z.D. Controlled enzymatic hydrolysis for improved exploitation of the antioxidant potential of wheat gluten. Ind. Crops Prod., 2017, 109, 548-557.
[http://dx.doi.org/10.1016/j.indcrop.2017.09.008]
[29]
Butré, C.I.; Sforza, S.; Gruppen, H.; Wierenga, P.A. Determination of the influence of substrate concentration on enzyme selectivity using whey protein Isolate and Bacillus licheniformis protease. J. Agric. Food Chem., 2014, 62(42), 10230-10239.
[http://dx.doi.org/10.1021/jf503151f ] [PMID: 25270540]
[30]
Hardt, N.A.; van der Goot, A.J.; Boom, R.M. Influence of high solid concentrations on enzymatic wheat gluten hydrolysis and resulting functional properties. J. Cereal Sci., 2013, 57(3), 531-536.
[http://dx.doi.org/10.1016/j.jcs.2013.03.006]
[31]
Chabanon, G.; Chevalot, I.; Framboisier, X.; Chenu, S.; Marc, I. Hydrolysis of rapeseed protein isolates: Kinetics, characterization and functional properties of hydrolysates. Process Biochem., 2007, 42(10), 1419-1428.
[http://dx.doi.org/10.1016/j.procbio.2007.07.009]
[32]
Deng, Y.; Butré, C.I.; Wierenga, P.A. Influence of substrate concentration on the extent of protein enzymatic hydrolysis. Int. Dairy J., 2018, 86, 39-48.
[http://dx.doi.org/10.1016/j.idairyj.2018.06.018]
[33]
Ng, K.; Rosenberg, A. Possible coupling of chemical to structural dynamics in subtilisin BPN’ catalyzed hydrolysis. Biophys. Chem., 1991, 39(1), 57-68.
[http://dx.doi.org/10.1016/0301-4622(91)85006-C] [PMID: 2012834]
[34]
Morales, J.A.; Figueroa, O.A.; Zapata, J.E. optimización de hidrólisis enzimática de la fracción globular de sangre bovina por metodología de superficie respuesta y evaluación de sus propiedades antioxidantes. Inf. Tecnol., 2017, 28(2), 75-86.
[http://dx.doi.org/10.4067/S0718-07642017000200009]
[35]
Vasquez, P.; Zapata Montoya, J.E. Optimization of enzymatic hydrolysis of viscera proteins of rainbow trout (Oncorhynchus mykiss). Adv. J. Food Sci. Technol., 2018, 16, 292-300.
[http://dx.doi.org/10.19026/ajfst.16.5970]
[36]
Butré, C.I.; Wierenga, P.A.; Gruppen, H. Effects of ionic strength on the enzymatic hydrolysis of diluted and concentrated whey protein isolate. J. Agric. Food Chem., 2012, 60(22), 5644-5651.
[http://dx.doi.org/10.1021/jf301409n ] [PMID: 22583537]
[37]
Linderstrøm-Lang, K. The initial phases of the enzymatic degradation of proteins. Bull. Soc. Chim. Biol. (Paris), 1953, 35(1-2), 100-116.
[PMID: 13042538]
[38]
Canabady-Rochelle, L.L.S.; Selmeczi, K.; Collin, S.; Pasc, A.; Muhr, L.; Boschi-Muller, S. SPR screening of metal chelating peptides in a hydrolysate for their antioxidant properties. Food Chem., 2018, 239, 478-485.
[http://dx.doi.org/10.1016/j.foodchem.2017.06.116] [PMID: 28873593]
[39]
Morales-Medina, R.; Pérez-Gálvez, R.; Guadix, A.; Guadix, E.M. Multiobjective optimization of the antioxidant activities of horse mackerel hydrolysates produced with protease mixtures. Process Biochem., 2017, 52, 149-158.
[http://dx.doi.org/10.1016/j.procbio.2016.11.001]
[40]
Nikoo, M.; Benjakul, S.; Yasemi, M.; Ahmadi Gavlighi, H.; Xu, X. Hydrolysates from rainbow trout (Oncorhynchus mykiss) processing by-product with different pretreatments: Antioxidant activity and their effect on lipid and protein oxidation of raw fish Emulsion. Lwt, 2019, 108, 120-128.
[http://dx.doi.org/10.1016/j.lwt.2019.03.049]
[41]
Alemán, A.; Giménez, B.; Pérez-Santin, E.; Gómez-Guillén, M.C.; Montero, P. Contribution of Leu and Hyp residues to antioxidant and ACE-inhibitory activities of peptide sequences isolated from squid gelatin hydrolysate. Food Chem., 2011, 125(2), 334-341.
[http://dx.doi.org/10.1016/j.foodchem.2010.08.058]
[42]
Intarasirisawat, R.; Benjakul, S.; Visessanguan, W.; Wu, J. Antioxidative and functional properties of protein hydrolysate from defatted skipjack (Katsuwonous pelamis) roe. Food Chem., 2012, 135(4), 3039-3048.
[http://dx.doi.org/10.1016/j.foodchem.2012.06.076] [PMID: 22980906]
[43]
Gómez, L.J.; Gómez, N.A.; Zapata, J.E.; López-García, G.; Cilla, A.; Alegría, A. In-vitro antioxidant capacity and cytoprotective/cytotoxic effects upon Caco-2 cells of red tilapia (Oreochromis spp.) viscera hydrolysates. Food Res. Int., 2019, 120, 52-61.
[http://dx.doi.org/10.1016/j.foodres.2019.02.029 ] [PMID: 31000267]
[44]
Jang, H.L.; Liceaga, A.M.; Yoon, K.Y. Purification, characterisation and stability of an antioxidant peptide derived from Sandfish (Arctoscopus japonicus). Protein hydrolysates. J. Funct. Foods, 2016, 20, 433-442.
[http://dx.doi.org/10.1016/j.jff.2015.11.020]
[45]
Wiriyaphan, C.; Xiao, H.; Decker, E.A.; Yongsawatdigul, J. Chemical and cellular antioxidative properties of threadfin bream (Nemipterus spp.) surimi byproduct hydrolysates fractionated by ultrafiltration. Food Chem., 2015, 167, 7-15.
[http://dx.doi.org/10.1016/j.foodchem.2014.06.077] [PMID: 25148952]
[46]
Batista, I.; Ramos, C.; Coutinho, J.; Bandarra, N.M.; Nunes, M.L. Characterization of protein hydrolysates and lipids obtained from Black Scabbardfish (Aphanopus carbo) by-products and antioxidative activity of the hydrolysates produced. Process Biochem., 2010, 45(1), 18-24.
[http://dx.doi.org/10.1016/j.procbio.2009.07.019]
[47]
Gómez, L.J.; Figueroa, O.A.; Zapata, J. Actividad antioxidante de hidrolizados enzimáticos de plasma bovino obtenidos por efecto de Alcalasa®2.4 L. Inf. Tecnol., 2013, 24, 33-42.
[http://dx.doi.org/10.4067/S0718-07642013000100005]
[48]
Sila, A.; Bougatef, A.; Nedjar-Arroume, N.; Manni, L.; Ravallec, R.; Barkia, A.; Guillochon, D.; Nasri, M.; Chi, C.F.; Hu, F.Y.; Wang, B.; Ren, X.J.; Deng, S.G.; Wu, C.W.; Girgih, A.T.; Udenigwe, C.C.; Hasan, F.M.; Gill, T.A.; Aluko, R.E.; Je, J.Y.; Park, S.Y.; Hwang, J.Y.; Ahn, C.B.; Jang, H.L.; Liceaga, A.M.; Yoon, K.Y.; Neves, A.C.; Harnedy, P.A.; O’Keeffe, M.B.; FitzGerald, R.J.; Song, R.; Zhang, K. qiang; Wei, R. bian; Zou, T. Bin; He, T.P.; Li, H. Bin; Tang, H.W.; Xia, E.Q. Amino acid composition and in vitro antioxidant and cytoprotective activity of abalone viscera hydrolysate. Food Chem., 2016, 21(1), 1674-1682.
[49]
Bourseau, P.; Vandanjon, L.; Jaouen, P.; Chaplain-Derouiniot, M.; Massé, A.; Guérard, F.; Chabeaud, A.; Fouchereau-Péron, M.; Le Gal, Y.; Ravallec-Plé, R.; Bergé, J-P.; Picot, L.; Piot, J-M.; Batista, I.; Thorkelsson, G.; Delannoy, C.; Jakobsen, G.; Johansson, I. Fractionation of fish protein hydrolysates by ultrafiltration and nanofiltration: impact on peptidic populations. Desalination, 2009, 244(1), 303-320.
[http://dx.doi.org/10.1016/j.desal.2008.05.026]
[50]
Liu, Y.; Li, X.; Chen, Z.; Yu, J.; Wang, F.; Wang, J. Characterization of structural and functional properties of fish protein hydrolysates from surimi processing by-products. Food Chem., 2014, 151, 459-465.
[http://dx.doi.org/10.1016/j.foodchem.2013.11.089] [PMID: 24423557]
[51]
Picot, L.; Ravallec, R.; Fouchereau-Péron, M.; Vandanjon, L.; Jaouen, P.; Chaplain-Derouiniot, M.; Guérard, F.; Chabeaud, A.; Legal, Y.; Alvarez, O.M.; Bergé, J-P.; Piot, J-M.; Batista, I.; Pires, C.; Thorkelsson, G.; Delannoy, C.; Jakobsen, G.; Johansson, I.; Bourseau, P. Impact of ultrafiltration and nanofiltration of an industrial fish protein hydrolysate on its bioactive properties. J. Sci. Food Agric., 2010, 90(11), 1819-1826.
[http://dx.doi.org/10.1002/jsfa.4020 ] [PMID: 20602518]
[52]
Saidi, S.; Deratani, A.; Ben Amar, R.; Belleville, M-P. Fractionation of a Tuna Dark muscle hydrolysate by a two-step membrane process. Separ. Purif. Tech., 2013, 108, 28-36.
[http://dx.doi.org/10.1016/j.seppur.2013.01.048]
[53]
Wang, B.; Li, L.; Chi, C-F.; Ma, J-H.; Luo, H-Y.; Xu, Y.F. Purification and characterisation of a novel antioxidant peptide derived from blue mussel (Mytilus edulis) protein hydrolysate. Food Chem., 2013, 138(2-3), 1713-1719.
[http://dx.doi.org/10.1016/j.foodchem.2012.12.002] [PMID: 23411302]
[54]
Hamzeh, A.; Benjakul, S.; Senphan, T. Comparative study on antioxidant activity of hydrolysates from splendid squid (Loligo formosana) gelatin and protein isolate prepared using protease from hepatopancreas of Pacific white shrimp (Litopenaeus vannamei). J. Food Sci. Technol., 2016, 53(9), 3615-3623.
[http://dx.doi.org/10.1007/s13197-016-2348-z ] [PMID: 27777469]
[55]
de Castro, R.J.S.; Sato, H.H. A Response surface approach on optimization of hydrolysis parameters for the production of egg white protein hydrolysates with antioxidant activities. Biocatal. Agric. Biotechnol., 2015, 4(1), 55-62.
[http://dx.doi.org/10.1016/j.bcab.2014.07.001]
[56]
Saidi, S.; Deratani, A.; Belleville, M-P.; Ben Amar, R. Production and fractionation of tuna by-product protein hydrolysate by ultrafiltration and nanofiltration: Impact on interesting peptides fractions and nutritional properties. Food Res. Int., 2014, 65, 453-461.
[http://dx.doi.org/10.1016/j.foodres.2014.04.026]
[57]
Gbogouri, G.A.; Linder, M.; Fanni, J.; Parmentier, M. Influence of hydrolysis degree on the functional properties of salmon byproducts hydrolysates. J. Food Sci., 2004, 69(8)
[http://dx.doi.org/10.1111/j.1365-2621.2004.tb09909.x]
[58]
Roslan, J.; Kamal, S.M.M.; Yunos, K.F.M.; Abdullah, N. A comparative study between Tilapia (Oreochromis niloticus) by-product and tilapia protein hydrolysate on Angiotensin I-Converting Enzyme (ACE) inhibition activities and functional properties. Sains Malays., 2018, 47(2), 309-318.
[59]
Villamil, O.; Váquiro, H.; Solanilla, J.F. Fish viscera protein hydrolysates: Production, potential applications and functional and bioactive properties. Food Chem., 2017, 224, 160-171.
[http://dx.doi.org/10.1016/j.foodchem.2016.12.057] [PMID: 28159251]
[60]
Kristinsson, H.G.; Rasco, B.A. Biochemical and functional properties of Atlantic salmon (Salmo salar) muscle proteins hydrolyzed with various alkaline proteases. J. Agric. Food Chem., 2000, 48(3), 657-666.
[http://dx.doi.org/10.1021/jf990447v ] [PMID: 10725130]

Rights & Permissions Print Cite
Article Metrics
21
© 2024 Bentham Science Publishers | Privacy Policy