Abstract
The current increase in the number of wastes produced by the shrimp industry has generated the need to find new methods to valorize such materials as they can be an important source of bioactive compounds while preserving the environment. In this study, proteins from Pacific white shrimp (Litopenaeus vannamei [Penaeus vannamei]) cooking juice (SCJP) were tested as a fermentation substrate for growth and protease production by the proteolytic strain Enterococcus faecalis DM19. This microorganism grew well and exhibited protease activity when cultivated in a medium containing only SCJP, indicating that the strain can obtain its carbon and nitrogen source requirements directly from shrimp waste protein. Also, the crude protease extract from Enterococcus faecalis DM19 was used to hydrolyze SCJP, and the antioxidant properties of the protein hydrolysate (SCJH) were investigated. The peptides and amino acids formed during the hydrolysis of shrimp waste protein are likely to be responsible for the antioxidant activity observed in this sample. The increased antioxidant activity of SCJH could be useful for the preservation of several products, especially in those cases in which oxidation processes are a limiting factor determining shelf-life.
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Cros, S., Lignot, B., Jaouen, P., Bourseau, P.: Technical and economical evaluation of an integrated membrane process capable both to produce an aroma concentrate and to reject clean water from shrimp cooking juices. J Food Eng. 77(3), 697–707 (2006)
Pérez-Santín, E., Calvo, M., López-Caballero, M., Montero, P., Gómez-Guillén, M.: Compositional properties and bioactive potential of waste material from shrimp cooking juice. LWT Food Sci. Technol. 54(1), 87–94 (2013)
Cai, L., Li, D., Dong, Z., Cao, A., Lin, H., Li, J.: Change regularity of the characteristics of Maillard reaction products derived from xylose and Chinese shrimp waste hydrolysates. LWT Food Sci. Technol. 65, 908–916 (2016)
Pihlanto, A., Korhonen, H.: Bioactive peptides from fermented foods and health promotion. In: Holzapfel, W. (ed.) Advances in fermented foods and beverages, pp. 39–74. Woodhead publishing Ltd., Cambridge, UK (2015)
Martone, C.B., Borla, O.P., Sánchez, J.J.: Fishery by-product as a nutrient source for bacteria and archaea growth media. Bioresour. Technol. 96(3), 383–387 (2005)
Aanand, S., Divya, M., Deepak, T., Padmavathi, P., Manimekalai, D.: Review on seafood processing plant wastewater bioremediation–A potential tool for waste management. IJAR 3(7), 01–04 (2017)
Martínez-Alvarez, O., Batista, I., Ramos, C., Montero, P.: Enhancement of ACE and prolyl oligopeptidase inhibitory potency of protein hydrolysates from sardine and tuna by-products by simulated gastrointestinal digestion. Food Funct. 7(4), 2066–2073 (2016)
Aranday-García, R., Guerrero, A.R., Ifuku, S., Shirai, K.: Successive inoculation of Lactobacillus brevis and Rhizopus oligosporus on shrimp wastes for recovery of chitin and added-value products. Process Biochem. 58, 17–24 (2017)
Martínez-Álvarez, O., López-Caballero, M., Gómez-Guillén, M., Montero, P.: Fermented seafood products and health. In: Frías, J., Martínez Villaluenga, C., Peñas, E. (eds.) Fermented foods in health and disease prevention, pp. 177–202. Academic Press, NY (2017)
Franz, C.M., Huch, M., Abriouel, H., Holzapfel, W., Galvez, A.: Enterococci as probiotics and their implications in food safety. Int. J. Food Microbiol. 151(2), 125–140 (2011)
Franz, C.M.A.P., Muscholl-Silberhorn, A.B., Yousif, N.M.K., Vancanneyt, M., Swings, J., Holzapfel, W.H.: Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl. Environ. Microb. 67, 4385–4389 (2001)
Giraffa, G., Carminati, D., Neviani, E.: Enterococci isolated from dairy products: a review of risks and potential technological use. J. Food Protect. 60, 732–738 (1997)
Djellouli, M., Martínez-Álvarez, O., Arancibia, M.Y., Florez-Cuadrado, D., Ugarte-Ruíz, M., Domínguez, L., Zadi-Karam, H., Karam, N., Roudj, S., López-Caballero, M.E.: Effect of seafood peptones on biomass and metabolic activity by Enterococcus faecalis DM19. LWT Food Sci. Technol. 81, 94–100 (2017)
Park, S.Y., Gibbs, B.F., Lee, B.H.: Effects of crude enzyme of Lactobacillus casei LLG on water-soluble peptides of enzyme-modified cheese. Food Res. Int. 28(1), 43–49 (1995)
Desmazeaud, M., Vassal, L.: Activité protéolytique intracellulaire de streptocoques lactiques mésophiles. Rôle au cours de l'affinage des fromages. Le lait 59(587), 327–344 (1979)
Adler-Nissen, J., Olsen, H.S.: The influence of peptide chain length on taste and functional properties of enzymatically modified soy protein. J. Chem. Technol. Biotechnol. 92, 125–146 (1979)
Lajmi, K., Gómez Estaca, J., Hammami, M., Martínez-Alvarez, O.: Upgrading collagenous smooth hound by-products: Effect of hydrolysis conditions, in vitro gastrointestinal digestion and encapsulation on bioactive properties. Food Biosci. 28, 99–108 (2019)
Djellouli, M., López-Caballero, M.E., Arancibia, M.Y., Karam, N., Martínez-Alvarez, O.: Antioxidant and antimicrobial enhancement by reaction of protein hydrolysates derived from shrimp by-products with glucosamine. Waste Biomass Valoriz. 11(6), 2491–2495 (2020)
Dinis, T.C., Madeira, V.M., Almeida, L.M.: Action of phenolic derivatives (acetaminophen, salicylate, and 5-aminosalicylate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Arch. Biochem. Biophys. 315(1), 161–169 (1994)
Mechri, S., Bouacem, K., Jabeur, F., Mohamed, S., Addou, N.A., Dab, A., Bouraoui, A., Bouanane-Darenfed, A., Bejar, S., Hacène, H.: Purification and biochemical characterization of a novel thermostable and halotolerant subtilisin SAPN, a serine protease from Melghiribacillus thermohalophilus Nari2A T for chitin extraction from crab and shrimp shell by-products. Extremophiles 23(5), 529–547 (2019)
Wang, S.-L., Chang, T.-J., Liang, T.-W.: Conversion and degradation of shellfish wastes by Serratia sp. TKU016 fermentation for the production of enzymes and bioactive materials. Biodegradation 21(3), 321–333 (2010)
Wang, S.-L., Yeh, P.-Y.: Production of a surfactant-and solvent-stable alkaliphilic protease by bioconversion of shrimp shell wastes fermented by Bacillus subtilis TKU007. Process Biochem. 41(7), 1545–1552 (2006)
Mechri, S., Sellem, I., Bouacem, K., Jabeur, F., Laribi-Habchi, H., Mellouli, L., Hacène, H., Bouanane-Darenfed, A., Jaouadi, B.: A biological clean processing approach for the valorization of speckled shrimp Metapenaeus monoceros by-product as a source of bioactive compounds. Environ. Sci. Pollut. Res. 1-14 (2020).
Sila, A., Martínez-Alvarez, O., Haddar, A., Gómez-Guillén, M.C., Nasri, M., Montero, M.P., Bougatef, A.: Recovery, viscoelastic and functional properties of Barbel skin gelatine: Investigation of anti-DPP-IV and anti-prolyl endopeptidase activities of generated gelatine polypeptides. Food Chem. 168, 478–486 (2015)
Martínez-Alvarez, O., Chamorro, S., Brenes, A.: Protein hydrolysates from animal processing by-products as a source of bioactive molecules with interest in animal feeding: a review. Food Res. Int. 73, 204–212 (2015)
Gómez-Guillén, C., López Caballero, M., Alemán, A., López de Lacey, A., Giménez, B., Montero García, P.: Antioxidant and antimicrobial peptide fractions from squid and tuna skin gelatin. In: Le Bihan, E., Koueta, N. (eds.) Sea by-products as a real material: New ways of application, pp. 89-115. Transworld Research Network, Kerala (2010).
Ruttanapornvareesakul, Y., Ikeda, M., Hara, K., Osatomi, K., Osako, K., Kongpun, O., Nozaki, Y.: Concentration-dependent suppressive effect of shrimp head protein hydrolysate on dehydration-induced denaturation of lizardfish myofibrils. Bioresour. Technol. 97(5), 762–769 (2006)
Gildberg, A., Stenberg, E.: A new process for advanced utilisation of shrimp waste. Process Biochem. 36(8–9), 809–812 (2001)
Mendis, E., Rajapakse, N., Byun, H.-G., Kim, S.-K.: Investigation of jumbo squid (Dosidicus gigas) skin gelatin peptides for their in vitro antioxidant effects. Life Sci. 77(17), 2166–2178 (2005)
Chen, H.-M., Muramoto, K., Yamauchi, F., Nokihara, K.: Antioxidant activity of designed peptides based on the antioxidative peptide isolated from digests of a soybean protein. J. Agric. Food. Chem. 44(9), 2619–2623 (1996)
Kim, S.-K., Mendis, E.: Bioactive compounds from marine processing byproducts–a review. Food Res. Int. 39(4), 383–393 (2006)
Kim, S.-K., Wijesekara, I.: Development and biological activities of marine-derived bioactive peptides: a review. J. Funct. Foods 2(1), 1–9 (2010)
Yang, J.-I., Ho, H.-Y., Chu, Y.-J., Chow, C.-J.: Characteristic and antioxidant activity of retorted gelatin hydrolysates from cobia (Rachycentron canadum) skin. Food Chem. 110(1), 128–136 (2008)
Phanturat, P., Benjakul, S., Visessanguan, W., Roytrakul, S.: Use of pyloric caeca extract from bigeye snapper (Priacanthus macracanthus) for the production of gelatin hydrolysate with antioxidative activity. LWT Food Sci. Technol. 43(1), 86–97 (2010)
Wu, H.-C., Chen, H.-M., Shiau, C.-Y.: Free amino acids and peptides as related to antioxidant properties in protein hydrolysates of mackerel (Scomber austriasicus). Food Res. Int. 36(9–10), 949–957 (2003)
Je, J.-Y., Park, P.-J., Kim, S.-K.: Antioxidant activity of a peptide isolated from Alaska pollack (Theragra chalcogramma) frame protein hydrolysate. Food Res. Int. 38(1), 45–50 (2005)
Balti, R., Bougatef, A., Sila, A., Guillochon, D., Dhulster, P., Nedjar-Arroume, N.: Nine novel angiotensin I-converting enzyme (ACE) inhibitory peptides from cuttlefish (Sepia officinalis) muscle protein hydrolysates and antihypertensive effect of the potent active peptide in spontaneously hypertensive rats. Food Chem. 170, 519–525 (2015)
Jo, H.-Y., Jung, W.-K., Kim, S.-K.: Purification and characterization of a novel anticoagulant peptide from marine echiuroid worm Urechis unicinctus. Process Biochem. 43(2), 179–184 (2008)
Liu, Z., Dong, S., Xu, J., Zeng, M., Song, H., Zhao, Y.: Production of cysteine-rich antimicrobial peptide by digestion of oyster (Crassostrea gigas) with alcalase and bromelin. Food Control 19(3), 231–235 (2008)
Theodore, A.E., Raghavan, S., Kristinsson, H.G.: Antioxidative activity of protein hydrolysates prepared from alkaline-aided channel catfish protein isolates. J. Agric. Food. Chem. 56(16), 7459–7466 (2008)
Alemán, A., Giménez, B., Montero, P., Gómez-Guillén, M.: Antioxidant activity of several marine skin gelatins. LWT Food Sci. Technol. 44(2), 407–413 (2011)
Bougatef, A., Nedjar-Arroume, N., Manni, L., Ravallec, R., Barkia, A., Guillochon, D., Nasri, M.: Purification and identification of novel antioxidant peptides from enzymatic hydrolysates of sardinelle (Sardinella aurita) by-products proteins. Food Chem. 118(3), 559–565 (2010)
Sila, A., Sayari, N., Balti, R., Martinez-Alvarez, O., Nedjar-Arroume, N., Moncef, N., Bougatef, A.: Biochemical and antioxidant properties of peptidic fraction of carotenoproteins generated from shrimp by-products by enzymatic hydrolysis. Food Chem. 148, 445–452 (2014)
Nasri, R., Jridi, M., Lassoued, I., Jemil, I., Salem, R.B.S.-B., Nasri, M., Karra-Châabouni, M.: The influence of the extent of enzymatic hydrolysis on antioxidative properties and ACE-inhibitory activities of protein hydrolysates from goby (Zosterisessor ophiocephalus) muscle. Appl. Biochem. Biotechol. 173(5), 1121–1134 (2014)
Himaya, S., Ryu, B., Ngo, D.-H., Kim, S.-K.: Peptide isolated from Japanese flounder skin gelatin protects against cellular oxidative damage. J. Agric. Food Chem. 60(36), 9112–9119 (2012)
Jao, C.-L., Ko, W.-C.: 1, 1-Diphenyl-2-picrylhydrazyl (DPPH) radical scavenging by protein hydrolyzates from tuna cooking juice. Fish Sci. 68(2), 430–435 (2002)
Vilailak, K., Soottawat, B., Duangporn, K., Fereidoon, S.: Antioxidative activity and functional properties of protein hydrolysate of yellow Stripe trevally (Selaroides leptolepis) as influenced by the degree of hydrolysis and enzyme type. Food Chem. 102(4), 1317–1327 (2007)
Ketnawa, S., Martínez-Alvarez, O., Benjakul, S., Rawdkuen, S.: Gelatin hydrolysates from farmed Giant catfish skin using alkaline proteases and its antioxidative function of simulated gastro-intestinal digestion. Food Chem. 192, 34–42 (2016)
Sun, J., Mao, X.: An environmental friendly process for Antarctic krill (Euphausia superba) utilization using fermentation technology. J. Clean. Prod. 127, 618–623 (2016)
Ghorbel-Bellaaj, O., Younes, I., Maâlej, H., Hajji, S., Nasri, M.: Chitin extraction from shrimp shell waste using Bacillus bacteria. Int. J. Biol. Macromol. 51(5), 1196–1201 (2012)
Nasri, R., Younes, I., Jridi, M., Trigui, M., Bougatef, A., Nedjar-Arroume, N., Dhulster, P., Nasri, M., Karra-Châabouni, M.: ACE inhibitory and antioxidative activities of Goby (Zosterissessor ophiocephalus) fish protein hydrolysates: effect on meat lipid oxidation. Food Res. Int. 54(1), 552–561 (2013)
Chen, H.-M., Muramoto, K., Yamauchi, F., Fujimoto, K., Nokihara, K.: Antioxidative properties of histidine-containing peptides designed from peptide fragments found in the digests of a soybean protein. J. Agric. Food. Chem. 46(1), 49–53 (1998)
Liñán-Cabello, M.A., Paniagua-Michel, J., Hopkins, P.M.: Bioactive roles of carotenoids and retinoids in crustaceans. Aquac. Nutr. 8(4), 299–309 (2002)
Wijesekara, I., Kim, S.-K.: Angiotensin-I-converting enzyme (ACE) inhibitors from marine resources: Prospects in the pharmaceutical industry. Mar. Drugs 8(4), 1080–1093 (2010)
Alashi, A.M., Blanchard, C.L., Mailer, R.J., Agboola, S.O., Mawson, A.J., He, R., Malomo, S.A., Girgih, A.T., Aluko, R.E.: Blood pressure lowering effects of Australian canola protein hydrolysates in spontaneously hypertensive rats. Food Res. Int. 55, 281–287 (2014)
Aluko, R.E., Girgih, A.T., He, R., Malomo, S., Li, H., Offengenden, M., Wu, J.: Structural and functional characterization of yellow field pea seed (Pisum sativum L.) protein-derived antihypertensive peptides. Food Res. Int. 77, 10–16 (2015)
Acknowledgements
This research was financed by the Spanish Ministry of Economy and Competitiveness (Project AGL2014-52825-R) and cofounded with European Union ERDF funds (European Regional Development Fund). Author M. Djellouli was funded by The National Centre of Biotechnology Research (CNRBt) of Algeria and the ENP (Exceptional National Program) Scholarship provided by the Ministry of Higher Education and Scientific Research of Algeria.
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Djellouli, M., López-Caballero, M.E., Roudj, S. et al. Hydrolysis of Shrimp Cooking Juice Waste for the Production of Antioxidant Peptides and Proteases by Enterococcus faecalis DM19. Waste Biomass Valor 12, 3741–3752 (2021). https://doi.org/10.1007/s12649-020-01263-3
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DOI: https://doi.org/10.1007/s12649-020-01263-3