Skip to main content
SpringerLink
Log in

Antioxidant and Antimicrobial Enhancement by Reaction of Protein Hydrolysates Derived from Shrimp By-Products with Glucosamine

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

Shrimp cooking juice and shrimp carapaces are interesting sources of protein which are habitually disposed of at large quantities by crustacean industries. In this work, protein obtained from the cooking juice and carapaces of Pacific white shrimp (Litopenaeus vannamei) was hydrolyzed by an enzyme extract of Enterococcus faecalis DM19 isolated from raw camel milk. The hydrolysates were afterwards heated separately with glucosamine (GlcN) at 100 °C for 0, 40, 60,120 and 180 min. The reaction was followed by measuring the change in absorbance at 294 and 420 nm and also by fluorescence (λexc = 340 nm; λem = 440 nm). Browning and intermediate products increased with heating time showing a concomitant decrease in free amino groups, while the pH decreased as well. Amino acid analysis showed that the amounts of lysine, arginine, and histidine decreased significantly after heating for 180 min. The infrared spectra suggested the appearance of new molecules after heating, presumably Schiff bases and/or aromatic compounds. The antioxidant and antimicrobial activities of the heated hydrolysates were compared to those of the native hydrolysates. Interestingly, the reducing ferric ion activity was improved 22-fold after conjugation. Meanwhile, both scavenging radical and metal chelating ion activities were increased sevenfold. Besides, the shrimp carapace hydrolysate heated in presence of GlcN exhibited a good antibacterial activity against gram positive and gram negative bacteria. To conclude, protein hydrolysates derived from the shrimp by-products studied in this work could be heated in presence of GlcN at 100 °C and be potentially used as antioxidant and/or antibacterial ingredients for different purposes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. FAO. FAO yearbook: Fishery and Aquaculture Statistics 2016. In: Publications. Rome, FAO of the United Nations (2018)

    Google Scholar 

  2. Ferraro, V., Cruz, I.B., Jorge, R.F., Malcata, F.X., Pintado, M.E., Castro, P.M.: Valorisation of natural extracts from marine source focused on marine by-products: a review. Food Res. Int. 43(9), 2221–2233 (2010)

    Google Scholar 

  3. Tonon, R.V., dos Santos, B.A., Couto, C.C., Mellinger-Silva, C., Brígida, A.I.S., Cabral, L.M.: Coupling of ultrafiltration and enzymatic hydrolysis aiming at valorizing shrimp wastewater. Food Chem. 198, 20–27 (2016)

    Google Scholar 

  4. Cahú, T.B., Santos, S.D., Mendes, A., Córdula, C.R., Chavante, S.F., Carvalho, L.B. Jr., Nader, H.B., Bezerra, R.S.: Recovery of protein, chitin, carotenoids and glycosaminoglycans from Pacific white shrimp (Litopenaeus vannamei) processing waste. Process Biochem. 47(4), 570–577 (2012)

    Google Scholar 

  5. Rai, A.K., Jini, R., Swapna, H., Sachindra, N., Bhaskar, N., Baskaran, V.: Application of native lactic acid bacteria (LAB) for fermentative recovery of lipids and proteins from fish processing wastes: bioactivities of fermentation products. J Aquat. Food Prod. Technol. 20(1), 32–44 (2011)

    Google Scholar 

  6. 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)

    Google Scholar 

  7. Murthy, P.S., Rai, A.K., Bhaskar, N.: Fermentative recovery of lipids and proteins from freshwater fish head waste with reference to antimicrobial and antioxidant properties of protein hydrolysate. J. Food Sci. Technol. 51(9), 1884–1892 (2014)

    Google Scholar 

  8. Mao, X., Zhang, J., Kan, F., Gao, Y., Lan, J., Zhang, X., Hu, Z., Li, Y., Lin, H.: Antioxidant production and chitin recovery from shrimp head fermentation with Streptococcus thermophilus. Food Sci. Biotechnol. 22(4), 1023–1032 (2013)

    Google Scholar 

  9. Martins, S.I., Jongen, W.M., Van Boekel, M.A.: A review of Maillard reaction in food and implications to kinetic modelling. Trends Food Sci. Technol. 11(9–10), 364–373 (2000)

    Google Scholar 

  10. Sanmartín, E., Arboleya, J.C., Villamiel, M., Moreno, F.J.: Recent advances in the recovery and improvement of functional proteins from fish processing by-products: use of protein Glycation as an alternative method. Compr. Rev. Food Sci. Food Saf. 8(4), 332–344 (2009)

    Google Scholar 

  11. Hrynets, Y., Ndagijimana, M., Betti, M.: Studies on the formation of Maillard and caramelization products from glucosamine incubated at 37 °C. J. Agric. Food Chem. 63(27), 6249–6261 (2015)

    Google Scholar 

  12. Jalal, A., Risheed, C., Ibrahim, B.: Optimization of chitin extraction from chicken feet. J. Anal. Bioanal. Tech. 3(5) (2012)

  13. Hrynets, Y., Ndagijimana, M., Betti, M.: Non-enzymatic glycation of natural actomyosin (NAM) with glucosamine in a liquid system at moderate temperatures. Food Chem. 139(1–4), 1062–1072 (2013)

    Google Scholar 

  14. Gómez-Estaca, J., Calvo, M., Álvarez-Acero, I., Montero, P., Gómez-Guillén, M.: Characterization and storage stability of astaxanthin esters, fatty acid profile and α-tocopherol of lipid extract from shrimp (L. vannamei) waste with potential applications as food ingredient. Food Chem. 216, 37–44 (2017)

    Google Scholar 

  15. 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)

    Google Scholar 

  16. Adler-Nissen, J.: A review of food hydrolysis specific area. In: Adler-Nissen, J. (ed.) Enzymatic hydrolysis of food protein, pp. 57–109. Elsevier, Copenhagen (1986)

    Google Scholar 

  17. Sumaya-Martinez, M., Thomas, S., Linard, B., Binet, A., Guerard, F.: Effect of Maillard reaction conditions on browning and antiradical activity of sugar–tuna stomach hydrolysate model system. Food Res. Int. 38(8–9), 1045–1050 (2005)

    Google Scholar 

  18. Ajandouz, E., Tchiakpe, L., Ore, F.D., Benajiba, A., Puigserver, A.: Effects of pH on caramelization and Maillard reaction kinetics in fructose-lysine model systems. J Food Sci. 66(7), 926–931 (2001)

    Google Scholar 

  19. Morales, F.J., Jimenez-Perez, S.: Free radical scavenging capacity of Maillard reaction products as related to colour and fluorescence. Food Chem. 72(1), 119–125 (2001)

    Google Scholar 

  20. Nielsen, P., Petersen, D., Dambmann, C.: Improved method for determining food protein degree of hydrolysis. J. Food Sci. 66(5), 642–646 (2001)

    Google Scholar 

  21. 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)

    Google Scholar 

  22. 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)

    Google Scholar 

  23. Arancibia, M., Giménez, B., López-Caballero, M., Gómez-Guillén, M., Montero, P.: Release of cinnamon essential oil from polysaccharide bilayer films and its use for microbial growth inhibition in chilled shrimps. LWT-Food Sci. Technol. 59(2), 989–995 (2014)

    Google Scholar 

  24. Jiang, Z., Wang, L., Che, H., Tian, B.: Effects of temperature and pH on angiotensin-I-converting enzyme inhibitory activity and physicochemical properties of bovine casein peptide in aqueous Maillard reaction system. LWT-Food Sci. Technol. 59(1), 35–42 (2014)

    Google Scholar 

  25. Brands, C.M., van Boekel, M.A.: Kinetic modeling of reactions in heated monosaccharide—casein systems. J. Agric. Food Chem. 50(23), 6725–6739 (2002)

    Google Scholar 

  26. Shu, C.-K.: Degradation products formed from glucosamine in water. J. Agric. Food Chem. 46(3), 1129–1131 (1998)

    Google Scholar 

  27. Eric, K., Raymond, L.V., Abbas, S., Song, S., Zhang, Y., Masamba, K., Zhang, X.: Temperature and cysteine addition effect on formation of sunflower hydrolysate Maillard reaction products and corresponding influence on sensory characteristics assessed by partial least square regression. Food Res. Int. 57, 242–258 (2014)

    Google Scholar 

  28. Lan, X., Liu, P., Xia, S., Jia, C., Mukunzi, D., Zhang, X., Xia, W., Tian, H., Xiao, Z.: Temperature effect on the non-volatile compounds of Maillard reaction products derived from xylose–soybean peptide system: Further insights into thermal degradation and cross-linking. Food Chem. 120(4), 967–972 (2010)

    Google Scholar 

  29. Van Chuyen, N., Kurata, T., Fujimaki, M.: Studies on the reaction of dipeptides with glyoxal. Agric. Biol. Chem. Tokyo 37(2), 327–334 (1973)

    Google Scholar 

  30. Corzo-Martínez, M., Montilla, A., Megías-Pérez, R., Olano, A., Moreno, F.J., Villamiel, M.: Impact of high-intensity ultrasound on the formation of lactulose and Maillard reaction glycoconjugates. Food Chem. 157, 186–192 (2014)

    Google Scholar 

  31. Poulsen, M.W., Hedegaard, R.V., Andersen, J.M., de Courten, B., Bügel, S., Nielsen, J., Skibsted, L.H., Dragsted, L.O.: Advanced glycation endproducts in food and their effects on health. Food Chem. Toxicol. 60, 10–37 (2013)

    Google Scholar 

  32. 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)

    Google Scholar 

  33. Renn, P.T., Sathe, S.K.: Effects of pH, temperature, and reactant molar ratio on l-leucine and d-glucose Maillard browning reaction in an aqueous system. J. Agric. Food Chem. 45(10), 3782–3787 (1997)

    Google Scholar 

  34. Kim, J.-S., Lee, Y.-S.: Study of Maillard reaction products derived from aqueous model systems with different peptide chain lengths. Food Chem. 116(4), 846–853 (2009)

    Google Scholar 

  35. Matiacevich, S.B., Buera, M.P.: A critical evaluation of fluorescence as a potential marker for the Maillard reaction. Food Chem. 95(3), 423–430 (2006)

    Google Scholar 

  36. Liu, J., Liu, M., He, C., Song, H., Chen, F.: Effect of thermal treatment on the flavor generation from Maillard reaction of xylose and chicken peptide. LWT-Food Sci. Technol. 64(1), 316–325 (2015)

    Google Scholar 

  37. Liu, P., Huang, M., Song, S., Hayat, K., Zhang, X., Xia, S., Jia, C.: Sensory characteristics and antioxidant activities of Maillard reaction products from soy protein hydrolysates with different molecular weight distribution. Food Bioprocess Technol. 5(5), 1775–1789 (2012)

    Google Scholar 

  38. Hong, P.K., Gottardi, D., Ndagijimana, M., Betti, M.: Glycation and transglutaminase mediated glycosylation of fish gelatin peptides with glucosamine enhance bioactivity. Food Chem. 142, 285–293 (2014)

    Google Scholar 

  39. Schmidt, R., Böhme, D., Singer, D., Frolov, A.: Specific tandem mass spectrometric detection of AGE-modified arginine residues in peptides. J. Mass Spectrom. 50(3), 613–624 (2015)

    Google Scholar 

  40. Benavente, M., Arias, S., Moreno, L., Martínez, J.: Production of glucosamine hydrochloride from crustacean shell. J. Pharm. Pharmacol. 3, 20–26 (2015)

    Google Scholar 

  41. Kong, J., Yu, S.: Fourier transform infrared spectroscopic analysis of protein secondary structures. Acta Biochem. Biophys. Sin. 39(8), 549–559 (2007)

    Google Scholar 

  42. Krimm, S., Bandekar, J.: Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv. Protein Chem. 38, 181–364 (1986)

    Google Scholar 

  43. Venyaminov, S.Y., Kalnin, N.: Quantitative IR spectrophotometry of peptide compounds in water (H2O) solutions. I. Spectral parameters of amino acid residue absorption bands. Biopolymers 30(13–14), 1243–1257 (1990)

    Google Scholar 

  44. Vhangani, L.N., Van Wyk, J.: Antioxidant activity of Maillard reaction products (MRPs) derived from fructose–lysine and ribose–lysine model systems. Food Chem. 137(1–4), 92–98 (2013)

    Google Scholar 

  45. Yen, G.-C., Chen, H.-Y.: Antioxidant activity of various tea extracts in relation to their antimutagenicity. J. Agric. Food Chem. 43(1), 27–32 (1995)

    Google Scholar 

  46. Yanagimoto, K., Lee, K.G., Ochi, H., Shibamoto, T.: Antioxidative activity of heterocyclic compounds formed in Maillard reaction products. Int. Congr. Ser. 1245, 335–340 (2002)

    Google Scholar 

  47. Hwang, I.G., Kim, H.Y., Woo, K.S., Lee, J., Jeong, H.S.: Biological activities of Maillard reaction products (MRPs) in a sugar–amino acid model system. Food Chem 126(1), 221–227 (2011)

    Google Scholar 

  48. Amarowicz, R.: Antioxidant activity of Maillard reaction products. Eur. J. Lipid Sci. Technol. 111(2), 109–111 (2009)

    Google Scholar 

  49. Eichner, K.: Antioxidative Effect of Maillard reaction intermediates. In: Simic, M.G., Karel, M. (eds.) Autoxidation in Food and Biological Systems. Springer, Boston (1980)

    Google Scholar 

  50. Yoshimura, Y., Iijima, T., Watanabe, T., Nakazawa, H.: Antioxidative effect of Maillard reaction products using glucose–glycine model system. J. Agric. Food Chem. 45(10), 4106–4109 (1997)

    Google Scholar 

  51. Kawakishi, S., Okawa, Y., Hayashi, T.: Interaction between melanoidin and active oxygen producing system. In: Ghee, A.H., Sze, L.W., Woo, F.C. (ed) Trends in Food Science: Proceedings of the 7th World Congress of Food Science and Technology, pp. 15–18. Singapore: Singapore Institute of Food Science and Technology: (1989)

  52. Matmaroh, K., Benjakul, S., Tanaka, M.: Effect of reactant concentrations on the Maillard reaction in a fructose–glycine model system and the inhibition of black tiger shrimp polyphenoloxidase. Food Chem. 98(1), 1–8 (2006)

    Google Scholar 

  53. Martinez, D.J.H.: Glucosamine and glucosamine-peptides antimicrobial compounds. https://era.library.ualberta.ca/items/34c8a68f-98f6-40be-9aef-f51539f064cf. Accessed 28 Dec 2018

  54. Maletta, A.B., Were, L.M.: Effect of coffee filtrate, methylglyoxal, glyoxal, and caffeine on Salmonella Typhimurium and S. Enteritidis survival in ground chicken breasts. J. Food Sci. 77(2), M135–M141 (2012)

    Google Scholar 

  55. Song, R., Yang, P., Wei, R., Ruan, G.: Antioxidative, antibacterial, and food functional properties of the half-fin anchovy hydrolysates-glucose conjugates formed via Maillard reaction. Molecules 21(6), 795 (2016)

    Google Scholar 

  56. Hiramoto, S., Itoh, K., Shizuuchi, S., Kawachi, Y., Morishita, Y., Nagase, M., Suzuki, Y., Nobuta, Y., Sudou, Y., Nakamura, O.: Melanoidin, a food protein-derived advanced Maillard reaction product, suppresses Helicobacter pylori in vitro and in vivo. Helicobacter 9(5), 429–435 (2004)

    Google Scholar 

  57. del Castillo, M.D., Ferrigno, A., Acampa, I., Borrelli, R.C., Olano, A., Martínez-Rodríguez, A., Fogliano, V.: In vitro release of angiotensin-converting enzyme inhibitors, peroxyl-radical scavengers and antibacterial compounds by enzymatic hydrolysis of glycated gluten. J Cereal Sci. 45(3), 327–334 (2007)

    Google Scholar 

  58. Lanciotti, R., Anese, M., Sinigaglia, M., Severini, C., Massini, R.: Effects of heated glucose-fructose-glutamic acid solutions on the growth of Bacillus stearothermophilus. LWT-Food Sci. Technol. 32(4), 223–230 (1999)

    Google Scholar 

  59. Rufian-Henares, J.A., de la Cueva, S.P.: Antimicrobial activity of coffee melanoidins: a study of their metal-chelating properties. J. Agric. Food Chem. 57(2), 432–438 (2009)

    Google Scholar 

Download references

Acknowledgements

This research was financed by the Spanish Ministry of Economy and Competitiveness (Projects AGL2011-27607, AGL2014-52825-R) and co-funded with European Union ERDF funds (European Regional Development Fund). Author M. Djellouli is funded by The National Centre of Biotechnology Research (CNRBt) of Algeria and ENP (Exceptional National Program) Scholarship provided by the Ministry of Higher Education and Scientific Research of Algeria. The authors thank J. Dolz, technician at ICTAN-CSIC, for his skill in the laboratory. Institute of Food Science, Technology and Nutrition (ICTAN-CSIC) has implemented and maintains a Quality Management System which fulfils the requirements of the ISO standard 9001:2015.

Author information

Authors and Affiliations

  1. Department of Food Biotechnology, Biotechnology Research Center, Ali Mendjeli, Nouvelle Ville, UV 03 BP E73, 25000, Constantine, Algeria

    Mustapha Djellouli

  2. Laboratory for Biology of Microorganisms and Biotechnology, Department of Biotechnology, Faculty of Sciences of Nature and Life, University of Oran 1 Ahmed Benbella, BP 1524, El-M’Naouer, 31000, Oran, Algeria

    Mustapha Djellouli & Noureddine Karam

  3. Institute of Food Science, Technology and Nutrition (ICTAN-CSIC), C/José Antonio Novais, 28040, Madrid, Spain

    M. Elvira López-Caballero & Oscar Martínez-Alvarez

  4. Technical University of Ambato (UTA), Av. Los Chasquis y Río Payamino, Ambato, Ecuador

    Mirari Y. Arancibia

Authors
  1. Mustapha Djellouli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Elvira López-Caballero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mirari Y. Arancibia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Noureddine Karam
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Oscar Martínez-Alvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Oscar Martínez-Alvarez.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Djellouli, M., López-Caballero, M.E., Arancibia, M.Y. et al. Antioxidant and Antimicrobial Enhancement by Reaction of Protein Hydrolysates Derived from Shrimp By-Products with Glucosamine. Waste Biomass Valor 11, 2491–2505 (2020). https://doi.org/10.1007/s12649-019-00607-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-019-00607-y

Keywords

Search

Navigation