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Enzymatic hydrolysis has been widely used to produce bioactive hydrolysates from sea cucumber body wall. Here, inspired by the clarification of Apostichopus japonicus genome, we investigated the enzymatic hydrolysis of sea cucumber body wall by using the omics strategy. Shared proteins, including major yolk proteins, collagens, extracellular matrix glycoproteins and muscle proteins, were released from the body wall by different hydrolysis condition. A portfolio of 216 shared peptides were detected in the peptidome by papain with different hydrolysis time, while 32 shared peptides were detected in the peptidome by differing proteases. Unshared peptides and the relative abundance distribution profiles of shared peptides changed depending on hydrolysis approaches, indicating dynamic changes of peptidome during hydrolysis. Moreover, release of sulfated fucan and fucosylated chondroitin sulfate changed with the hydrolysis condition. The monitoring of dynamic enzymatic hydrolysis process at a molecular scale would contribute to production and quality control of sea cucumber hydrolysates.


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Dynamic changes of peptidome and release of polysaccharide in sea cucumber (Apostichopus japonicus) hydrolysates depending on enzymatic hydrolysis approaches

Show Author's information Yanchao WangaYan SongaYaoguang Changa,b( )Yanyan LiuaGuangning ChenaChanghu Xuea,b
College of Food Science and Engineering, Ocean University of China, Qingdao 266003, China
Laboratory for Marine Drugs and Bioproducts, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China

Abstract

Enzymatic hydrolysis has been widely used to produce bioactive hydrolysates from sea cucumber body wall. Here, inspired by the clarification of Apostichopus japonicus genome, we investigated the enzymatic hydrolysis of sea cucumber body wall by using the omics strategy. Shared proteins, including major yolk proteins, collagens, extracellular matrix glycoproteins and muscle proteins, were released from the body wall by different hydrolysis condition. A portfolio of 216 shared peptides were detected in the peptidome by papain with different hydrolysis time, while 32 shared peptides were detected in the peptidome by differing proteases. Unshared peptides and the relative abundance distribution profiles of shared peptides changed depending on hydrolysis approaches, indicating dynamic changes of peptidome during hydrolysis. Moreover, release of sulfated fucan and fucosylated chondroitin sulfate changed with the hydrolysis condition. The monitoring of dynamic enzymatic hydrolysis process at a molecular scale would contribute to production and quality control of sea cucumber hydrolysates.

Keywords: Protein, Polysaccharide, Enzymatic hydrolysis, Sea cucumber, Peptidome

References(41)

[1]

S. Bordbar, F. Anwar, N. Saari, High-value components and bioactives from sea cucumbers for functional foods-A review, Mar. Drugs 9 (2011) 1761-1805. https://doi.org/10.3390/md9101761.

[2]

M. Fabinyi, Historical, cultural and social perspectives on luxury seafood consumption in China, Environ. Conserv. 39 (2012) 83-92. https://doi.org/10.1017/S0376892911000609.

[3]
Fishery Bureau of the Ministry of Agriculture. China Agriculture Press: Beijing 2018.
[4]

J. Wen, C.Q. Hu, S.G. Fan, Chemical composition and nutritional quality of sea cucumbers. J. Sci. Food Agric. 90 (2010) 2469-2474. https://doi.org/10.1002/jsfa.4108.

[5]

X.Q. Zhou, C.H. Wang, A.L. Jiang, Antioxidant peptides isolated from sea cucumber Stichopus japonicus, Eur. Food Res. Technol. 234 (2012) 441-447. https://doi.org/10.1007/s00217-011-1610-x.

[6]

J.A. Pérez-Vega, L. Olivera-Castillo, J. Á. Gómez-Ruiz, et al., Release of multifunctional peptides by gastrointestinal digestion of sea cucumber (Isostichopus badionotus), J. Funct. Foods 5 (2013) 869-877. https://doi.org/10.1016/j.jff.2013.01.036.

[7]

Y.Y. Li, J. Shang, Z.Z. Jiang, et al., Regulation mechanism of peptides derived from sea cucumber (Apostichopus japonicas) for modulation of learning and memory, Food Sci. Biotechnol. 25 (2016) 241-246. https://doi.org/10.1007/s10068-016-0035-5.

[8]

N. Sun, P.B. Cui, Z.Q. Jin, et al., Contributions of molecular size, charge distribution, and specific amino acids to the iron-binding capacity of sea cucumber (Stichopus japonicus) ovum hydrolysates, Food Chem. 230 (2017)627-636. https://doi.org/10.1016/j.foodchem.2017.03.077.

[9]

X.L. Lin, M.J. Yao, J.H. Lu, et al., Identification of novel oligopeptides from the simulated digestion of sea cucumber (Stichopus japonicus) to alleviate Aβ aggregation progression, J. Funct. Foods 60 (2019) 103412. https://doi.org/10.1016/j.jff.2019.06.014.

[10]

J. Wang, Y.G. Chang, F.X. Wu, et al., Fucosylated chondroitin sulfate is covalently associated with collagen fibrils in sea cucumber Apostichopus japonicus body wall, Carbohydr. Polym. 186 (2018) 439-444. https://doi.org/10.1016/j.carbpol.2018.01.041.

[11]

M. Tian, C.H. Xue, Y.G. Chang, et al., Collagen fibrils of sea cucumber(Apostichopus japonicus) are heterotypic, Food Chem. 316 (2020) 126272. https://doi.org/10.1016/j.foodchem.2020.126272.

[12]

P.W.M.L.H.K. Marambe, P.J. Shand, J.P.D. Wanasundara, An in-vitro investigation of selected biological activities of hydrolysed flaxseed (Linum usitatissimum L.) proteins, J. Am. Oil. Chem. Soc. 85 (2008) 1155-1164. https://doi.org/10.1007/s11746-008-1293-z.

[13]

M. Karamać, A. Kosińska-Cagnazzo, A. Kulczyk, Use of different proteases to obtainflaxseed protein hydrolysates with antioxidant activity, Int. J. Mol. Sci. 17 (2016) 1027-1039. https://doi.org/10.3390/ijms17071027.

[14]

L.Z. Lin, K. Yang, L. Zheng, et al., Anti-aging effect of sea cucumber(Cucumaria frondosa) hydrolysate on fruit flies and d-galactose-induced aging mice, J. Funct. Foods 47 (2018) 11-18. https://doi.org/10.1016/j.jff.2018.05.033.

[15]

T.Y. Zhou, X.W. Xiang, M. Du, et al., Protective effect of polysaccharides of sea cucumber Acaudina leucoprocta on hydrogen peroxide-induced oxidative injury in RAW264.7 cells, Int. J. Biol. Macromol. 139 (2019)1133-1140. https://doi.org/10.1016/j.ijbiomac.2019.08.092.

[16]

L. Yan, D. Wang, Y. Yu, et al., Fucosylated chondroitin sulfate 9-18 oligomers exhibit molecular size-independent antithrombotic activity while circulating in the blood, ACS Chem. Biol. 15 (2020) 2232-2246. https://doi.org/10.1021/acschembio.0c00439.

[17]

I.P.S. Fernando, K.K.A. Sanjeewa, K.W. Samarakoon, et al., A fucoidan fraction purified from Chnoospora minima; a potential inhibitor of LPS-induced inflammatory responses, Int. J. Biol. Macromol. 104 (2017) 1185-1193. https://doi.org/10.1016/j.ijbiomac.2017.07.031.

[18]

Y.C. Wang, W. Su, C. Y, Zhang, et al., Protective effect of sea cucumber(Acaudina molpadioides) fucoidan against ethanol-induced gastric damage, Food Chem. 133 (2012) 1414-1419. https://doi.org/10.1016/j.foodchem.2012.02.028.

[19]

X.J. Zhang, L.N. Sun, J.B. Yuan, et al., The sea cucumber genome provides insights into morphological evolution and visceral regeneration, PLoS Biol. 15 (2017). https://doi.org/10.1371/journal.pbio.2003790.

[20]

O.H. Lowry, N.J. Rosebrough, A.L. Farr, et al., Protein measurement with the Folin phenol reagent, J. Biol. Chem. 193 (1951) 265-275.

[21]

R.W. Farndale, D.J. Buttle, A.J. Barrett, Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue, Biochim. Biophys. Acta Gen. Subj. 883 (1986) 173-177. https://doi.org/10.1016/0304-4165(86)90306-5.

[22]

D.J. Strydom, Chromatographic-separation of 1-phenyl-3-methyl-5-pyrazolone-derivatized neutral, acidic and basic aldoses, J. Chromatogr. A 678 (1994) 17-23. https://doi.org/10.1016/0021-9673(94)87069-1.

[23]

N. Khaldi, V. Vijayakumar, D.C. Dallas, et al., Predicting the important enzymes in human breast milk digestion, J. Agric. Food Chem. 62 (2014)7225-7232. https://doi.org/10.1021/jf405601e.

[24]

B. Manavalan, S. Basith, T.H. Shin, et al., mAHTPred: a sequence-based meta-predictor for improving the prediction of anti-hypertensive peptides using effective feature representation, Bioinformatics 35 (2019) 2757-2765. https://doi.org/10.1093/bioinformatics/bty1047.

[25]

Y.C. Wang, M. Tian, Y.G. Chang, et al., Investigation of structural proteins in sea cucumber (Apostichopus japonicus) body wall, Sci. Rep. 10 (2020)18744. https://doi.org/10.1038/s41598-020-75580-x.

[26]

L. Tripoteau, G. Bedoux, J. Gagnon, et al., In vitro antiviral activities of enzymatic hydrolysates extracted from byproducts of the Atlantic holothurian Cucumaria frondosa, Process. Biochem. 50 (2015) 867-875. https://doi.org/10.1016/j.procbio.2015.02.012.

[27]

S. Beaubier, X. Framboisier, I. Ioannou, et al., Simultaneous quantification of the degree of hydrolysis, protein conversion rate and mean molar weight of peptides released in the course of enzymatic proteolysis, J. Chromatogr. B 1105 (2019) 1-9. https://doi.org/10.1016/j.jchromb.2018.12.005.

[28]

M. Saito, N. Kunisaki, N. Urano, et al., Collagen as the major edible component of sea cucumber (Stichopus japonicus), J. Food Sci. 67 (2002)1319-1322. https://doi.org/10.1111/j.1365-2621.2002.tb10281.x.

[29]

A. Fujiwara, T. Unuma, K. Ohno, et al., Molecular characterization of the major yolk protein of the Japanese common sea cucumber (Apostichopus japonicus) and its expression profile during ovarian development, Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 155 (2010) 34-40. https://doi.org/10.1016/j.cbpa.2009.09.002.

[30]

J.M. Brooks, G.M. Wessel, The major yolk protein in sea urchins is a transferrin-like, iron binding protein, Dev. Biol. 245 (2002) 1-12. https://doi.org/10.1006/dbio.2002.0611.

[31]

J. Kim, S.H. Moon, D.U. Ahn, et al., Antioxidant effects of ovotransferrin and its hydrolysates, Poult. Sci. 91 (2012) 2747-2754. https://doi.org/10.3382/ps.2012-02150.

[32]

X. Wang, Y. Zhao, Y. Yao, et al., Anti-inflammatory activity of di-peptides derived from ovotransferrin by simulated peptide-cut in TNF-α-induced Caco-2 cells, J. Funct. Foods 37 (2017) 424-432. https://doi.org/10.1016/j.jff.2017.07.064.

[33]

B. Ma, Y. Guo, X. Fu, et al., Identification and antimicrobial mechanisms of a novel peptide derived from egg white ovotransferrin hydrolysates, LWT-Food Sci. Technol. 131 (2020) 109720. https://doi.org/10.1016/j.lwt.2020.109720.

[34]

O.L. Tavano, Protein hydrolysis using proteases: an important tool for food biotechnology, J. Mol. Catal. B Enzym. 90 (2013) 1-11. https://doi.org/10.1016/j.molcatb.2013.01.011.

[35]

H.L. Wu, Y.Q. Hu, J.D. Shen, et al., Identification of a novel gelatinolytic metalloproteinase (GMP) in the body wall of sea cucumber (Stichopus japonicus) and its involvement in collagen degradation, Process Biochem. 48(2013) 871-877. https://doi.org/10.1016/j.procbio.2013.04.011.

[36]

H.T. Wu, D.M. Li, B.W. Zhu, et al., Proteolysis of noncollagenous proteins in sea cucumber, Stichopus japonicus, body wall: characterisation and the effects of cysteine protease inhibitors, Food Chem. 141 (2013) 1287-1294. https://doi.org/10.1016/j.foodchem.2013.03.088.

[37]

Y.X. Liu, D.Y. Zhou, D.D. Ma, et al., Changes in collagenous tissue microstructures and distributions of cathepsin L in body wall of autolytic sea cucumber (Stichopus japonicus), Food Chem. 212 (2016) 341-348. https://doi.org/10.1016/j.foodchem.2016.05.173.

[38]

C.P. Yu, Y. Cha, F. Wu, et al., Molecular cloning and functional characterization of cathepsin D from sea cucumber Apostichopus japonicus, Fish. Shellfish. Immun. 70 (2017) 553-559. https://doi.org/10.1016/j.fsi.2017.09.011.

[39]

Y.C. Gu, J.P. Wu, The potential of antioxidative and anti-inflammatory peptides in reducing the risk of cardiovascular diseases, Curr. Opin. Food Sci. 8 (2016) 25-32. https://doi.org/10.1016/j.cofs.2016.01.011.

[40]

Z. Shahi, S.Z. Sayyed-Alangi, L. Najafian, Effects of enzyme type and process time on hydrolysis degree, electrophoresis bands and antioxidant properties of hydrolyzed proteins derived from defatted Bunium persicum Bioss. press cake, Heliyon 6 (2020) e03365. https://doi.org/10.1016/j.heliyon.2020.e03365.

[41]

J. Tkaczewska, J. Borawska-Dziadkiewicz, P. Kulawik, et al., The effects of hydrolysis condition on the antioxidant activity of protein hydrolysate from Cyprinus carpio skin gelatin, LWT-Food Sci. Technol. 117 (2020) 108616. https://doi.org/10.1016/j.lwt.2019.108616.

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Received: 14 November 2020
Revised: 28 December 2020
Accepted: 23 January 2021
Published: 02 June 2022
Issue date: September 2022

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© 2022 Beijing Academy of Food Sciences.

Acknowledgements

Acknowledgement

This work was supported by the Fok Ying-Tong Education Foundation (171024), Fundamental Research Funds for the Central Universities (201941005) and Fundamental Research Funds for the Central Universities (862001013136).

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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