Regulatory mechanism of ι-carrageenan oligosaccharides in coordination with calcium ions on the thermal gelation of sea cucumber collagen

Abstract

Sea cucumbers suffer from non-enzymatic deterioration during heat processing and storage, which significantly devaluates the product. In the present investigation, it was found that ι-carrageenan oligosaccharide (ι-CO) synergized with Ca²⁺ is able to protect sea cucumbers from deterioration. The textural strength and water-holding capacity of the sea cucumber body wall were improved after treatment with ι-CO and Ca²⁺, and the collagen structure was more resistant to destructive experiments. In addition, pepsin-solubilized sea cucumber collagen (SCC) was extracted and demonstrated that the positive effect was due to co-gelation between ι-CO and collagen supported by rheological and thermal property studies. Furthermore, molecular dynamics simulations confirmed that ι-CO spontaneously binds to SCC, while Ca²⁺ promotes the crosslinking strength of the ι-CO-SCC mixed gel and enhances its water-holding capacity and mechanical strength. Therefore, the ι-CO/Ca²⁺ can permeate and stabilize collagen hydrogel, which provides valuable information for the development of new food additives to improve the texture of collagen-based foods.

Keywords

Sea cucumber / Deterioration / Thermal stability / ι-carrageenan oligosaccharides / Molecular dynamics simulation

References

[1] BordbarS, AnwarF, SaariN. High-value components and bioactives from sea cucumbers for functional foods - a review. Mar Drugs, 2011, 9(10): 1761-1805.

[2] HuangX, WangH, TuZ. A comprehensive review of the control and utilization of aquatic animal products by autolysis-based processes: mechanism, process, factors, and application. Food Res Int, 2023, 164. 112325

[3] GuoQ, SunDW, ChengJH, HanZ. Microwave processing techniques and their recent applications in the food industry. Trends Food Sci Technol, 2017, 67: 236-247.

[4] LiuJ, XuY, XiaT, XueC, LiuL, ChangP, WangD, SunX. Oxidized oligosaccharides stabilize rehydrated sea cucumbers against high-temperature impact. Int J Mol Sci, 2020, 21(15): 1-13.

[5] YuJ, GeW, WangK, HaoW, YangS, XuY, FengT, HanP, SunX. Crosslinking ability of hydrolyzed distarch phosphate and its stabilizing effect on rehydrated sea cucumber. Food Chem, 2024, 456. 139866

[6] HuY, DuL, SunY, ZhouC, PanD. Recent developments in phosphorylation modification on food proteins: structure characterization, site identification and function. Food Hydrocoll, 2023, 137. 108390

[7] YanX, ChenY, DanW, DanN, LiZ. Bletilla striata polysaccharide modified collagen fiber composite sponge with rapid hemostasis function. Collagen & Leather, 2022, 5(1): 2097-1419.

[8] LiS, LangS, ChenZ, ChenJ, ZhuangW, DuY, YaoY, LiuG, ChenM. Polyphenol based hybrid nano-aggregates modified collagen fibers of biological valve leaflets to achieve enhanced mechanical, anticoagulation and anti-calcification properties. Collagen & Leather, 2022, 4(1): 2097-1419.

[9] QiX, SunX, ZhuL, ZhangH, WangY, LiuY, HouH. Intervention mechanism of self-degradation of ready-to-eat sea cucumber by adding green tea extract and gallic acid. Food Res Int, 2022, 156. 111282

[10] LiuZ, LiD, SongL, LiuY, YuM, ZhangM, RakariyathamK, ZhouD, ShahidiF. Effects of proteolysis and oxidation on mechanical properties of sea cucumber ( stichopus japonicus ) during thermal processing and storage and their control. Food Chem, 2020, 330. 127248

[11] CaoH, LiuD, ZhiL, LiuJ, LiuY, XuH, WangD, XuY, XueC, SunX. Oxidized inositol stabilizes rehydrated sea cucumbers against non-enzymatic deterioration. Food Chem, 2023, 405. 134973

[12] CaoH, LiuY, ZhiL, JingS, LiZ, WangD, XuY, SunX. Inhibitory effect of pre-gelatinized dialdehyde starch on heat-induced deterioration of sea cucumber. J Sci Food Agric, 2023, 103(6): 2848-2857.

[13] LiuY, YuJ, CaoH, XueC, ChenK, XuY, SunX. The cross-linking ability of dialdo-galactose in food processing condition. Food Chem, 2024, 433. 137356

[14] ShuiS, YangH, LuB, ZhangB. Phosphorylated trehalose suppresses the denaturation of myofibrillar proteins in peeled shrimp (litopenaeus vannamei) during long-term frozen storage. Foods, 2022, 11203189.

[15] MakshakovaON, ZuevYF. Interaction-induced structural transformations in polysaccharide and protein-polysaccharide gels as functional basis for novel soft-matter: a case of carrageenans. Gels, 2022.

[16] ElbandyM. Anti-inflammatory effects of marine bioactive compounds and their potential as functional food ingredients in the prevention and treatment of neuroinflammatory disorders. Molecules, 2023, 2812.

[17] ZhuB, NiF, XiongQ, YaoZ. Marine oligosaccharides originated from seaweeds: source, preparation, structure, physiological activity and applications. Crit Rev Food Sci Nutr, 2021, 61(1): 60-74.

[18] WangY, LiuT, XieJ, ChengM, SunL, ZhangS, XinJ, ZhangN. A review on application of molecular simulation technology in food molecules interaction. Curr Res Food Sci, 2022, 5: 1873-1881.

[19] YuJ, HaoW, DiH, LiK, XuY, SunX, XueC. Stabilizing effect of hydrolyzed distarch phosphate on litopenaeus vannamei myofibrillar protein hydrogel and products. Food Hydrocoll, 2025, 162. 110902

[20] SunX, ZhuL, QiX, ZhangH, WuL, WangJ, HouH. Cleavage sites and non-enzymatic self-degradation mechanism of ready-to-eat sea cucumber during storage. Food Chem, 2022, 375. 131722

[21] FarooqS, AhmadM, ZhengS, AliU, LiY, ShiX, ZhangH. A review on marine collagen: sources, extraction methods, colloids properties, and food applications. Collagen & Leather, 2024, 6111.

[22] YuB, GongX, ZhangN, BenjakulS, ZhangY, FuY. Glycation modification of protein hydrolysate from channel catfish ( ictalurus punetaus ) viscera to mitigate undesirable flavor: unraveling structure and flavor characteristics. Food Chem X, 2024, 24. 101993

[23] ZhangQ, LiuR, GeirsdóttirM, LiS, TomassonT, XiongS, LiX, GudjónsdóttirM. Thermal-induced autolysis enzymes inactivation, protein degradation and physical properties of sea cucumber, cucumaria frondosa. Processes, 2022, 105847.

[24] LiuW, TianZ, LiC, LiG. Thermal denaturation of fish collagen in solution: a calorimetric and kinetic analysis. Thermochim Acta, 2014, 581: 32-40.

[25] NarayananP, JanardhananS. An approach towards identification of leather from leather-like polymeric material using ftir-atr technique. Collagen & Leather, 2024, 6111.

[26] WangH, KeL, DingY, RaoP, XuT, HanH, ZhouJ, DingW, ShangX. Effect of calcium ions on rheological properties and structure of lycium barbarum L. polysaccharide and its gelation mechanism. Food Hydrocoll, 2022, 122. 107079

[27] YinS, ZhangY, ZhangX, TaoK, LiG. High-strength collagen/delphinidin film incorporated with vaccinium oxycoccus pigment for active and intelligent food packaging. Collagen & Leather, 2023, 5111.

[28] NecasJ, BartosikovaL. Carrageenan: a review. Veterinarni Med, 2013, 58(4): 187-205.

[29] BannwarthC, EhlertS, GrimmeS. GFN2-XTB - an accurate and broadly parametrized self-consistent tight-binding quantum chemical method with multipole electrostatics and density-dependent dispersion contributions. J Chem Theory Comput, 2019, 15(3): 1652-1671.

[30] PanF, LiX, TuersuntuohetiT, WangW, ZhengX, FangX, TianW, PengW. Molecular mechanism of high-pressure processing regulates the aggregation of major royal jelly proteins. Food Hydrocolloids., 2023, 144108928.

[31] ZhangX, XuS, ShenL, LiG. Factors affecting thermal stability of collagen from the aspects of extraction, processing and modification. J Leather Sci Eng, 2020, 21. 19

[32] WuJ, LiaoW, ZhangJ, ChenW. Thermal behavior of collagen crosslinked with tannic acid under microwave heating. J Therm Anal Calorim, 2019, 135: 2329-2335.

[33] LiuY, TianX, ZhangF, ZhangW. Probing the topological effects on stability enhancement and therapeutic performance of protein bioconjugates: tadpole, macrocycle versus figure-of-eight. Adv Healthc Mater, 2024, 13. 2400466

[34] SiL, FanY, WangY, SunL, LiB, XueC, HouH. Thermal degradation behavior of collagen from sea cucumber (Stichopus japonicus) using TG-FTIR analysis. Thermochim Acta, 2018, 659: 166-171.

[35] MiH, LiY, WangC, YiS, LiX, LiJ. The interaction of starch-gums and their effect on gel properties and protein conformation of silver carp surimi. Food Hydrocoll, 2021, 112. 106290

[36] XuX, XuJ, ZhangY, ZhangL. Rheology of triple helical lentinan in solution: steady shear viscosity and dynamic oscillatory behavior. Food Hydrocolloids, 2008, 22: 735-741.

[37] FengX, YuX, YangY, TangX. Improving the freeze-thaw stability of fish myofibrils and myofibrillar protein gels: current methods and future perspectives. Food Hydrocoll, 2023, 144. 109041

[38] GeQ, RongS, YinC, McClementsDJ, FuQ, LiQ, HanY, LiuF, WangS, ChenS. Calcium ions induced ι-carrageenan-based gel-coating deposited on zein nanoparticles for encapsulating the curcumin. Food Chem, 2024, 434. 137488

[39] YanJ, YinL, QuY, YanW, ZhangM, SuJ, JiaX. Effect of calcium ions concentration on the properties and microstructures of doubly induced sorghum arabinoxylan/soy protein isolate mixed gels. Food Hydrocoll, 2022, 133. 107997

[40] OnofrioA, ParisiG, PunziG, TodiscoS, Di NoiaMA, BossisF, TuriA, De GrassiA, PierriCL. Distance-dependent hydrophobic-hydrophobic contacts in protein folding simulations. Phys Chem Chem Phys, 2014, 16(35): 18907-18917.

Funding

Innovative Research Group Project of the National Natural Science Foundation of China(U22A20542)

National Key Research and Development Program of China(2023YFF1103800)

RIGHTS & PERMISSIONS

The Author(s)