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Effect of L-Lysine on Heat-Induced Aggregation Behavior of Antarctic Krill (Euphausia superba) Myofibrillar Protein

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Abstract

Heat treatment reduces the quality of Antarctic krill (Euphausia superba) meat, thus greatly limiting its industrial application. It was found that L-Lys immersion pretreatment can effectively improve the quality of heat-treated Antarctic krill meat; the underlying mechanism is unclear. Therefore, this study aimed to investigate the effect of L-Lys concentrations (0, 25, 50, 100, and 200 mM) on the aggregation behavior and structure of Antarctic krill myofibrillar protein solution before and after heat treatment. Compared with the untreated group, L-Lys decreased the surface hydrophobicity and particle size of the heat-treated Antarctic krill protein by 2.38 times and 18.27 times while increasing the solubility by 3.59 times. Furthermore, L-Lys intervention inhibited the formation of disulfide bonds in myofibrillar protein of the heat-treated Antarctic krill, enhanced the intermolecular hydrogen bonding force, improved the orderliness of the secondary structure, and “exposed” the tyrosine residues of the protein molecule. As a result, the polarity of the microenvironment was enhanced while the tertiary structure of the protein was altered, thus inhibiting thermal aggregation. This study reveals the mechanism of L-Lys inhibition of thermal aggregation behavior of Antarctic krill myofibrillar protein. Our results provide insights into the development and utilization of Antarctic krill protein in the food industry.

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All data generated or analyzed during this study are included in this published article.

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References

  • Atkinson, A., Siegel, V., Pakhomov, E. A., Jessopp, M. J., & Loeb, V. (2009). A re-appraisal of the total biomass and annual production of Antarctic krill. Deep Sea Research Part I: Oceanographic Research Papers, 56(5), 727–740. https://doi.org/10.1016/j.dsr.2008.12.007

    Article  Google Scholar 

  • Bao, P., Chen, L., Wang, Y., Hu, Y., & Zhou, C. J. M. S. (2021). Quality of frozen porcine Longissimus lumborum muscles injected with L-arginine and L-lysine solution. Meat Science, 179, 108530. https://doi.org/10.1016/j.meatsci.2021.108530

  • Bao, P., Chen, L., Hu, Y., Wang, Y., & Zhou, C. (2022). l-Arginine and l-lysine retard aggregation and polar residue modifications of myofibrillar proteins: Their roles in solubility of myofibrillar proteins in frozen porcine Longissimus lumborum. Food Chemistry, 393, 133347. https://doi.org/10.1016/j.foodchem.2022.133347

  • Barut Gök, S. (2021). UV-C Treatment of apple and grape juices by modified UV-C reactor based on Dean vortex technology: Microbial, physicochemical and sensorial parameters evaluation. Food and Bioprocess Technology, 14(6), 1055–1066. https://doi.org/10.1007/s11947-021-02624-z

    Article  CAS  Google Scholar 

  • Buamard, N., & Benjakul, S. (2017). Cross-linking activity of ethanolic coconut husk extract toward sardine (Sardinella albella) muscle proteins. Journal of Food Biochemistry, 41(2), e12283. https://doi.org/10.1111/jfbc.12283

  • Cai, L., Feng, J., Cao, A., Tian, H., Wang, J., Liu, Y., Gong, L., & Li, J. (2018). Effect of partial substitutes of NaCl on the cold-set gelation of grass carp myofibrillar protein mediated by microbial transglutaminase. Food and Bioprocess Technology, 11(10), 1876–1886. https://doi.org/10.1007/s11947-018-2149-7

    Article  CAS  Google Scholar 

  • Cao, Y., Li, B., Fan, X., Wang, J., Zhu, Z., Huang, J., & Xiong, Y. L. (2021). Synergistic recovery and enhancement of gelling properties of oxidatively damaged myofibrillar protein by l-lysine and transglutaminase. Food Chemistry, 358, 129860. https://doi.org/10.1016/j.foodchem.2021.129860

  • Cavan, E. L., Belcher, A., Atkinson, A., Hill, S. L., Kawaguchi, S., McCormack, S., Meyer, B., Nicol, S., Ratnarajah, L., Schmidt, K., Steinberg, D. K., Tarling, G. A., & Boyd, P. W. (2019). The importance of Antarctic krill in biogeochemical cycles. Nature Communications, 10(1), 4742. https://doi.org/10.1038/s41467-019-12668-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, M., Wang, L., Xie, B., Ma, A., Hu, K., Zheng, C., Xiong, G., Shi, L., Ding, A., Li, X., Qiao, Y., Sun, Z., & Wu, W. (2022). Effects of high-pressure treatments (ultra-high hydrostatic pressure and high-pressure homogenization) on bighead carp (Aristichthys nobilis) myofibrillar protein native state and its hydrolysate. Food and Bioprocess Technology, 15(10), 2252–2266. https://doi.org/10.1007/s11947-022-02878-1

    Article  CAS  Google Scholar 

  • Chen, X., Xiong, Y. L., & Xu, X. (2019). High-pressure homogenization combined with sulfhydryl blockage by hydrogen peroxide enhance the thermal stability of chicken breast myofibrillar protein aqueous solution. Food Chemistry, 285, 31–38. https://doi.org/10.1016/j.foodchem.2019.01.131

    Article  CAS  PubMed  Google Scholar 

  • Cueto, M., Farroni, A., Rodríguez, S. D., Schoenlechner, R., Schleining, G., & del Pilar, B. M. (2018). Assessing changes in enriched maize flour formulations after extrusion by means of FTIR, XRD, and chemometric analysis. Food and Bioprocess Technology, 11(8), 1586–1595. https://doi.org/10.1007/s11947-018-2113-6

    Article  CAS  Google Scholar 

  • Ding, Y., Liu, R., Rong, J., & Xiong, S. (2014). Heat-induced denaturation and aggregation of actomyosin and myosin from yellowcheek carp during setting. Food Chemistry, 149, 237–243. https://doi.org/10.1016/j.foodchem.2013.10.123

    Article  CAS  PubMed  Google Scholar 

  • Du, Y.-N., Han, J.-R., Yin, Z.-K., Yan, J.-N., Jiang, X.-Y., & Wu, H.-T. (2021). Conjugation of (–)-epigallocatechin-3-gallate and protein isolate from large yellow croaker (Pseudosciaena crocea) roe: Improvement of antioxidant activity and structural characteristics. Journal of the Science of Food and Agriculture, 101(14), 5948–5955. https://doi.org/10.1002/jsfa.11247

    Article  CAS  PubMed  Google Scholar 

  • Fadimu, G. J., Gill, H., Farahnaky, A., & Truong, T. (2021). Investigating the impact of ultrasound pretreatment on the physicochemical, structural, and antioxidant properties of lupin protein hydrolysates. Food and Bioprocess Technology, 14(11), 2004–2019. https://doi.org/10.1007/s11947-021-02700-4

    Article  CAS  Google Scholar 

  • Fu, Y., Zheng, Y., Lei, Z., Xu, P., & Zhou, C. (2017). Gelling properties of myosin as affected by L-lysine and L-arginine by changing the main molecular forces and microstructure. International Journal of Food Properties, 20, S884-S898. https://doi.org/10.1080/10942912.2017.1315593

  • Guo, X. Y., Peng, Z. Q., Zhang, Y. W., Liu, B., & Cui, Y. Q. (2015). The solubility and conformational characteristics of porcine myosin as affected by the presence of l-lysine and l-histidine. Food Chemistry, 170, 212–217. https://doi.org/10.1016/j.foodchem.2014.08.045

    Article  CAS  PubMed  Google Scholar 

  • Grewe, J., & Schwarz, U. S. (2020). Mechanosensitive self-assembly of myosin II minifilaments. Physical Review E, 101(2), 022402. https://doi.org/10.1103/PhysRevE.101.022402

  • Hassoun, A., Aït-Kaddour, A., Sahar, A., & Cozzolino, D. (2021). Monitoring thermal treatments applied to meat using traditional methods and spectroscopic techniques: A review of advances over the last decade. Food and Bioprocess Technology, 14(2), 195–208. https://doi.org/10.1007/s11947-020-02510-0

    Article  Google Scholar 

  • Huang, M., Mao, Y., Li, H., & Yang, H. (2021). Kappa-carrageenan enhances the gelation and structural changes of egg yolk via electrostatic interactions with yolk protein. Food Chemistry, 360, 129972. https://doi.org/10.1016/j.foodchem.2021.129972

  • Igual, M., Contreras, C., Camacho, M. M., & Martínez-Navarrete, N. (2014). Effect of thermal treatment and storage conditions on the physical and sensory properties of grapefruit juice. Food and Bioprocess Technology, 7(1), 191–203. https://doi.org/10.1007/s11947-013-1088-6

    Article  CAS  Google Scholar 

  • Jia, D., Huang, Q., & Xiong, S. (2016). Chemical interactions and gel properties of black carp actomyosin affected by MTGase and their relationships. Food Chemistry, 196, 1180–1187. https://doi.org/10.1016/j.foodchem.2015.10.030

    Article  CAS  PubMed  Google Scholar 

  • Li, Z., Sun, Q., Zheng, Y., Wang, J., Tian, Y., Zheng, B., & Guo, Z. (2020). Effect of two-step microwave heating on the gelation properties of golden threadfin bream (Nemipterus virgatus) myosin. Food Chemistry, 328, 127104. https://doi.org/10.1016/j.foodchem.2020.127104

  • Liang, Y., Guo, B., Zhou, A., Xiao, S., & Liu, X. (2017). Effect of high pressure treatment on gel characteristics and gel formation mechanism of bighead carp (Aristichthys nobilis) surimi gels. Journal of Food Processing and Preservation, 41(5), e13155. https://doi.org/10.1111/jfpp.13155

  • Lin, J., Zhang, Y., Li, Y., Sun, P., Ren, X., & Li, D. (2022). Improving the texture properties and protein thermal stability of Antarctic krill (Euphausia superba) by L-lysine marination. Journal of the Science of Food and Agriculture, 102(9), 3916–3924. https://doi.org/10.1002/jsfa.11741

    Article  CAS  PubMed  Google Scholar 

  • Liu, H., Zhang, H., Liu, Q., Chen, Q., & Kong, B. (2020). Solubilization and stable dispersion of myofibrillar proteins in water through the destruction and inhibition of the assembly of filaments using high-intensity ultrasound. Ultrasonics Sonochemistry, 67, 105160. https://doi.org/10.1016/j.ultsonch.2020.105160

  • Mao, W., Li, X., Fukuoka, M., Liu, S., Ji, H., & Sakai, N. (2016). Study of Ca2+-ATPase activity and solubility in the whole kuruma prawn (Marsupenaeus japonicus) meat during heating: Based on the kinetics analysis of myofibril protein thermal denaturation. Food and Bioprocess Technology, 9(9), 1511–1520. https://doi.org/10.1007/s11947-016-1739-5

    Article  CAS  Google Scholar 

  • Ngarize, S., Adams, A., & Howell, N. K. (2004). Studies on egg albumen and whey protein interactions by FT-Raman spectroscopy and rheology. Food Hydrocolloids, 18(1), 49–59. https://doi.org/10.1016/S0268-005X(03)00041-9

    Article  CAS  Google Scholar 

  • Panpipat, W., & Chaijan, M. (2020). Effect of atmospheric pressure cold plasma on biophysical properties and aggregation of natural actomyosin from threadfin bream (Nemipterus bleekeri). Food and Bioprocess Technology, 13(5), 851–859. https://doi.org/10.1007/s11947-020-02441-w

    Article  CAS  Google Scholar 

  • Qin, H., Xu, P., Zhou, C., & Wang, Y. (2015). Effects of l-arginine on water holding capacity and texture of heat-induced gel of salt-soluble proteins from breast muscle. LWT - Food Science and Technology, 63(2), 912–918. https://doi.org/10.1016/j.lwt.2015.04.048

    Article  CAS  Google Scholar 

  • Qiu, C., Xia, W., & Jiang, Q. (2014). Pressure-induced changes of silver carp (Hypophthalmichthys molitrix) myofibrillar protein structure. European Food Research and Technology, 238(5), 753–761. https://doi.org/10.1007/s00217-014-2155-6

    Article  CAS  Google Scholar 

  • Stefanović, A. B., Jovanović, J. R., Dojčinović, M. B., Lević, S. M., Nedović, V. A., Bugarski, B. M., & Knežević-Jugović, Z. D. (2017). Effect of the controlled high-intensity ultrasound on improving functionality and structural changes of egg white Proteins. Food and Bioprocess Technology, 10(7), 1224–1239. https://doi.org/10.1007/s11947-017-1884-5

    Article  CAS  Google Scholar 

  • Sun, P., Lin, J., Ren, X., Zhang, B., Liu, J., Zhao, Y., & Li, D. (2022). Effect of heating on protein denaturation, water state, microstructure, and textural properties of Antarctic krill (Euphausia superba) meat. Food and Bioprocess Technology, 15(10), 2313–2326. https://doi.org/10.1007/s11947-022-02881-6

    Article  CAS  Google Scholar 

  • Sun, P., Zhang, X., Ren, X., Cao, Z., Zhao, Y., Man, H., & Li, D. (2023). Effect of basic amino acid pretreatment on the quality of canned Antarctic krill. Food and Bioprocess Technology, 16(8), 1690–1702. https://doi.org/10.1007/s11947-023-03027-y

    Article  CAS  Google Scholar 

  • Thorarinsdottir, K. A., Arason, S., Geirsdottir, M., Bogason, S. G., & Kristbergsson, K. (2002). Changes in myofibrillar proteins during processing of salted cod (Gadus morhua) as determined by electrophoresis and differential scanning calorimetry. Food Chemistry, 77(3), 377–385. https://doi.org/10.1016/S0308-8146(01)00349-1

    Article  CAS  Google Scholar 

  • Turgay-İzzetoğlu, G., Çokgezme, Ö. F., Döner, D., Ersoy, C., Çabas, B. M., & İçier, F. (2022). Cooking the chicken meat with moderate electric field: Rheological properties and image processing of microstructure. Food and Bioprocess Technology, 15(5), 1082–1100. https://doi.org/10.1007/s11947-022-02800-9

    Article  CAS  Google Scholar 

  • Vate, N. K., & Benjakul, S. (2016). Combined effect of squid ink tyrosinase and tannic acid on heat induced aggregation of natural actomyosin from sardine. Food Hydrocolloids, 56, 62–70. https://doi.org/10.1016/j.foodhyd.2015.12.009

  • Wachirasiri, K., Wanlapa, S., Uttapap, D., & Rungsardthong, V. (2016). Use of amino acids as a phosphate alternative and their effects on quality of frozen white shrimps (Penaeus vanamei). LWT - Food Science and Technology, 69, 303–311. https://doi.org/10.1016/j.lwt.2016.01.065

  • Wagner, J., Biliaderis, C. G., & Moschakis, T. (2020). Whey proteins: Musings on denaturation, aggregate formation and gelation. Critical Reviews in Food Science and Nutrition, 60(22), 3793–3806. https://doi.org/10.1080/10408398.2019.1708263

  • Wang, K.-Q., Luo, S.-Z., Zhong, X.-Y., Cai, J., Jiang, S.-T., & Zheng, Z. (2017). Changes in chemical interactions and protein conformation during heat-induced wheat gluten gel formation. Food Chemistry, 214, 393–399. https://doi.org/10.1016/j.foodchem.2016.07.037

  • Wang, S., Shi, Y., Tu, Z., Zhang, L., Wang, H., Tian, M., & Zhang, N. (2017). Influence of soy lecithin concentration on the physical properties of whey protein isolate-stabilized emulsion and microcapsule formation. Journal of Food Engineering, 207, 73–80. https://doi.org/10.1016/j.jfoodeng.2017.03.020

    Article  CAS  Google Scholar 

  • Xia, M., Chen, Y., Guo, J., Feng, X., Yin, X., Wang, L., Wu, W., Li, Z., Sun, W., & Ma, J. (2019). Effects of oxidative modification on textural properties and gel structure of pork myofibrillar proteins. Food Research International, 121, 678–683. https://doi.org/10.1016/j.foodres.2018.12.037

  • Yang, Y., Wang, Q., Tang, Y., Lei, L., Zhao, J., Zhang, Y., Li, L., Wang, Q., & Ming, J. (2021). Effects of ionic strength and (−)-epigallocatechin gallate on physicochemical characteristics of soybean 11S and 7S proteins. Food Hydrocolloids, 119, 106836. https://doi.org/10.1016/j.foodhyd.2021.106836

  • Yu, N., Xu, Y., Jiang, Q., & Xia, W. (2017). Molecular forces involved in heat-induced freshwater surimi gel: Effects of various bond disrupting agents on the gel properties and protein conformation changes. Food Hydrocolloids, 69, 193–201. https://doi.org/10.1016/j.foodhyd.2017.02.003

    Article  CAS  Google Scholar 

  • Zhang, F., Jiang, S., Feng, X., Wang, R., Zeng, M., & Zhao, Y. (2020). Physicochemical state and in vitro digestibility of heat treated water-soluble protein from Pacific oyster (Crassostrea gigas). Food Bioscience, 34, 100528. https://doi.org/10.1016/j.fbio.2020.100528

  • Zhang, D., Zhang, Y., Huang, Y., Chen, L., Bao, P., Fang, H., & Zhou, C. (2021). l-Arginine and l-lysine alleviate myosin from oxidation: Their role in maintaining myosin’s Emulsifying Properties. Journal of Agricultural and Food Chemistry, 69(10), 3189–3198. https://doi.org/10.1021/acs.jafc.0c06095

  • Zhang, M., Qiu, W., Zhang, R., Row, K., Cheng, Y., & Jin, Y. (2017a). Effect of amino acids on microwave dielectric properties of minced Antarctic krill (Euphausia superba). Food and Bioprocess Technology, 10(10), 1809–1823. https://doi.org/10.1007/s11947-017-1952-x

    Article  CAS  Google Scholar 

  • Zhang, Z., Yang, Y., Zhou, P., Zhang, X., & Wang, J. (2017b). Effects of high pressure modification on conformation and gelation properties of myofibrillar protein. Food Chemistry, 217, 678–686. https://doi.org/10.1016/j.foodchem.2016.09.040

    Article  CAS  PubMed  Google Scholar 

  • Zhao, Q., Yu, X., Zhou, C., Yagoub, A. E. A., & Ma, H. (2020). Effects of collagen and casein with phenolic compounds interactions on protein in vitro digestion and antioxidation. LWT, 124, 109192. https://doi.org/10.1016/j.lwt.2020.109192

  • Zhao, X., Chen, F., Xue, W., & Lee, L. (2008). FTIR spectra studies on the secondary structures of 7S and 11S globulins from soybean proteins using AOT reverse micellar extraction. Food Hydrocolloids, 22(4), 568–575. https://doi.org/10.1016/j.foodhyd.2007.01.019

    Article  CAS  Google Scholar 

  • Zheng, Y. J. I. J. O. N., & Sciences, F. (2017). Effects of L-lysine/L-arginine on the physicochemical properties and quality of sodium-reduced and phosphate-free pork sausage. International Journal of Nutrition and Food Sciences, 6(1), 12. https://doi.org/10.19026/ajfst.6.91

  • Zheng, H., Beamer, S. K., Matak, K. E., & Jaczynski, J. (2019). Effect of κ-carrageenan on gelation and gel characteristics of Antarctic krill (Euphausia superba) protein isolated with isoelectric solubilization/precipitation. Food Chemistry, 278, 644–652. https://doi.org/10.1016/j.foodchem.2018.11.080

    Article  CAS  PubMed  Google Scholar 

  • Zielinska, S., Cybulska, J., Pieczywek, P., Zdunek, A., Kurzyna-Szklarek, M., Staniszewska, I., Liu, Z.-L., Pan, Z., Xiao, H.-W., & Zielinska, M. (2022). Structural morphology and rheological properties of pectin fractions extracted from okra pods subjected to cold plasma treatment. Food and Bioprocess Technology, 15(5), 1168–1181. https://doi.org/10.1007/s11947-022-02798-0

    Article  CAS  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (32372364) and the National Key Research and Development Project of Dalian (Grant No. 2022YF16SN033).

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Authors and Affiliations

  1. School of Food Science and Technology, National Engineering Research Center of Seafood, Dalian Polytechnic University, Dalian , Liaoning, 116034, China

    Junxin Lin, Peizi Sun, Yanfen Zhao, Xiang Ren, Hao Man & Dongmei Li

  2. Liaoyu Group Co., Ltd., Dalian, 116034, Liaoning, China

    Xiaoping Du

  3. Engineering Research Center of Seafood of Ministry of Education of China, Dalian, 116034, Liaoning, China

    Dongmei Li

  4. Collaborative Innovation Center of Seafood Deep Processing, Dalian Polytechnic University, Dalian, 116034, Liaoning, China

    Dongmei Li

  5. State Key Laboratory of Marine Food Processing and Safety Control, Dalian, 116034, Liaoning, China

    Dongmei Li

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  1. Junxin Lin
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  2. Peizi Sun
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  3. Yanfen Zhao
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Contributions

Junxin Lin: methodology, investigation, and writing—original draft. Peizi Sun: conceptualization, methodology, and investigation. Yanfen Zhao: investigation and methodology. Xiaoping Du: investigation. Xiang Ren: investigation. Hao Man: investigation and methodology. Dongmei Li: conceptualization, supervision, and writing—review and editing.

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Lin, J., Sun, P., Zhao, Y. et al. Effect of L-Lysine on Heat-Induced Aggregation Behavior of Antarctic Krill (Euphausia superba) Myofibrillar Protein. Food Bioprocess Technol 17, 1448–1461 (2024). https://doi.org/10.1007/s11947-023-03205-y

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