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Review | Publishing Language: Chinese | Open Access

Research Progress on Fucoidan-Degrading Enzymes

Zhen WEI1,2,3 ()Jinling CHEN1,2Jie YANG1,2
Jiangsu Key Laboratory of Marine Living Resources and Environment, Jiangsu Ocean University, Lianyungang 222005, China
Co-innovation Center of Jiangsu Marine Bio-industry Technology, Lianyungang 222005, China
Jiangsu Institute of Marine Resources Development, Lianyungang 222005, China
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Abstract

Fucoidan-degrading enzymes are glycoside hydrolases that hydrolyze fucoidan into low molecular mass fucosan with biological activity or other products. The enzymes have great application value in the preparation of active fucoidan oligosaccharides, biopharmaceutics and disease diagnosis. In this article, the sources, properties, modes of action, structures and applications of fucoidan-degrading enzymes are reviewed, revealing that fucoidan-degrading enzymes are mainly derived from marine microorganisms and marine invertebrates and that the enzymatic properties, substrate specificity, molecular structures and catalytic mechanisms of fucoidan-degrading enzymes vary significantly depending on the species source. Different types of fucoidan-degrading enzymes catalyze different sites of complex fucoidans producing fucoidan oligosaccharides with antioxidant, anti-tumor, anti-thrombotic or other special activities. Therefore, the utilization of fucoidan-degrading enzymes in the preparation of drugs and functional foods has gradually become a research focus in the application field of polysaccharides. This article provides theoretical support for further research on fucoidan-degrading enzymes, and also provides references for the effective development of fucoidan oligosaccharides with special biological functions.

CLC number: Q936 Document code: A Article ID: 1002-6630(2024)09-0306-08

References

[1]

KUSAYKIN M I, SILCHENKO A S, ZAKHARENKO A M, et al. Fucoidanases[J]. Glycobiology, 2016, 26(1): 3-12. DOI:10.1093/glycob/cwv072.

[2]

AMIN M L, MAWAD D, DOKOS S, et al. Immunomodulatory properties of photopolymerizable fucoidan and carrageenans[J]. Carbohydrate Polymers, 2020, 230: 115691. DOI:10.1016/j.carbpol.2019.115691.

[3]

SENTHILKUMAR K, KIM S K. Anticancer effects of fucoidan[J]. Advances in Food and Nutrition Research, 2014, 72: 195-213. DOI:10.1016/B978-0-12-800269-8.00011-7.

[4]

WANG L, JAYAWARDENA T U, HYUN J, et al. Antioxidant and antiphotoaging effects of a fucoidan isolated from Turbinaria ornata[J]. International Journal of Biological Macromolecules, 2023, 225: 1021-1027. DOI:10.1016/j.ijbiomac.2022.11.164.

[5]

CHEN Q R, KOU L Y, WANG F W, et al. Size-dependent whitening activity of enzyme-degraded fucoidan from Laminaria japonica[J]. Carbohydrate Polymers, 2019, 225: 115211. DOI:10.1016/j.carbpol.2019.115211.

[8]

BRUHN A, JANICEK T, MANNS D, et al. Crude fucoidan content in two north Atlantic kelp species, Saccharina latissima and Laminaria digitata-seasonal variation and impact of environmental factors[J]. Journal of Applied Phycology, 2017, 29(6): 3121-3137. DOI:10.1007/s10811-017-1204-5.

[9]

ZAYED A, EL-AASR M, IBRAHIM A S, et al. Fucoidan characterization: determination of purity and physicochemical and chemical properties[J]. Marine Drugs, 2020, 18(11): 571. DOI:10.3390/md18110571.

[10]

LI B, LU F, WEI X J, et al. Fucoidan: structure and bioactivity[J]. Molecules, 2008, 13(8): 1671-1695. DOI:10.3390/molecules13081671.

[11]

JAYAWARDENA T U, NAGAHAWATTA D P, FERNANDO I P S, et al. A review on fucoidan structure, extraction techniques, and its role as an immunomodulatory agent[J]. Marine Drugs, 2022, 20(12): 755. DOI:10.3390/md20120755.

[12]

YAPHE W, MORGAN K. Enzymic hydrolysis of fucoidin by Pseudomonas atlantica and Pseudomonas carrageenovora[J]. Nature, 1959, 183: 761-762. DOI:10.1038/183761b0.

[13]

THANASSP N M, NAKADA H I. Enzymic degradation of fucoidan by enzymes from the hepatopancreas of abalone, Haliotus species[J]. Archives of Biochemistry and Biophysics, 1967, 118: 172-177. DOI:10.1016/0003-9861(67)90294-9.

[14]

TRANG V T D, MIKKELSEN M D, VUILLEMIN M, et al. The endoalpha(1,4) specific fucoidanase Fhf2 from Formosa haliotis releases highly sulfated fucoidan oligosaccharides[J]. Frontiers in Plant Science, 2022, 13: 823668. DOI:10.3389/fpls.2022.823668.

[15]

IVANOVAE P, SAWABE T, ALEXEEVA Y V, et al. Pseudoalteromonas issachenkonii sp. nov., a bacterium that degrades the thallus of the brown alga Fucus evanescens[J]. International Journal of Systematic and Evolutionary Microbiology, 2002, 52: 229-234. DOI:10.1099/00207713-52-1-229.

[16]

ZHU C L, LIU Z B, REN L S, et al. Overexpression and biochemical characterization of a truncated endo-alpha (1→3)-fucoidanase from Alteromonas sp. SN-1009[J]. Food Chemistry, 2021, 353: 129460. DOI:10.1016/j.foodchem.2021.129460.

[17]

TRAN V H N, NGUYEN T T, MEIER S, et al. The endo-α(1,3)-fucoidanase Mef2 releases uniquely branched oligosaccharides from Saccharina latissima fucoidans[J]. Marine Drugs, 2022, 20(5): 305. DOI:10.3390/md20050305.

[18]

KIM W, PARK J, PARK J, et al. Purification and characterization of a fucoidanase (FNase S) from a marine bacterium Sphingomonas paucimobilis PF-1[J]. Marine Drugs, 2015, 13(7): 4398-4417. DOI:10.3390/md13074398.

[19]

VUILLEMIN M, SILCHENKO A S, CAO H T T, et al. Functional characterization of a new GH107 endo-alpha-(1,4)-fucoidanase from the marine bacterium Formosa haliotis[J]. Marine Drugs, 2020, 18(11): 562. DOI:10.3390/md18110562.

[20]

ZUEVA A O, SILCHENKO A S, RASIN A B, et al. Expression and biochemical characterization of two recombinant fucoidanases from the marine bacterium Wenyingzhuangia fucanilytica CZ1127T[J]. International Journal of Biological Macromolecules, 2020, 164: 3025-3037. DOI:10.1016/j.ijbiomac.2020.08.131.

[21]

ARAI Y, SHINGU Y, YAGI H, et al. Occurrence of different fucoidanase genes in Flavobacterium sp. SW and enzyme characterization[J]. Journal of Bioscience and Bioengineering, 2022, 134(3): 187-194. DOI:10.1016/j.jbiosc.2022.06.003.

[22]

LIU S, WANG Q K, SHAO Z W, et al. Purification and characterization of the enzyme fucoidanase from Cobetia amphilecti utilizing fucoidan from Undaria pinnatifida[J]. Foods, 2023, 12(7): 1555. DOI:10.3390/foods12071555.

[23]

WU Q Q, MA S, XIAO H R, et al. Purification and the secondary structure of fucoidanase from Fusarium sp. LD8[J]. Evidence-based Complementary and Alternative Medicine, 2011, 2011: 196190. DOI:10.1155/2011/196190.

[24]

WU Q Q, ZHANG M, WU K, et al. Purification and characteristics of fucoidanase obtained from Dendryphiella arenaria TM94[J]. Journal of Applied Phycology, 2010, 23(2): 197-203. DOI:10.1007/s10811-010-9588-5.

[26]

KITAMURA K, MATSUO M, TSUNEO Y. Enzymic degradation of fucoidan by fucoidanase from the hepatopancreas of Patinopecten yessoensis[J]. Bioscience Biotechnology and Biochemistry, 1992, 56(3): 490-494. DOI:10.1271/bbb.56.490.

[27]

SASAKI K, SAKAI T, KOJIMA K, et al. Partial purification and characterization of an enzyme releasing 2-sulfo-α-L-fucopyranose from 2-sulfo-α-L-fucopyranosyl-(1→2) pyridylaminated fucose from a sea urchin, Strongylocentrotus nudus[J]. Bioscience Biotechnology and Biochemistry, 1996, 60(4): 666-668. DOI:10.1271/BBB.60.666.

[28]

BILAN M I, KUSAYKIN M I, GRACHEV A A, et al. Effect of enzyme preparation from the marine mollusk Littorina kurila on fucoidan from the brown alga Fucus distichus[J]. Biochemistry, 2005, 70(12): 1321-1326. DOI:10.1007/s10541-005-0264-3.

[29]

WU H Y, OWEN C D, JUGE N. Structure and function of microbial α-L-fucosidases: a mini review[J]. Essays in Biochemistry 2023, 67(3): 399-414. DOI:10.1042/EBC20220158.

[30]

COBUCCI-PONZANO B, CONTE F, ROSSI M, et al. The alpha-L-fucosidase from Sulfolobus solfataricus[J]. Extremophiles, 2008, 12(1): 61-68. DOI:10.1007/s00792-007-0105-y.

[31]

SILCHENKO A S, RUBTSOV N K, ZUEVA A O, et al. Fucoidanactive alpha-L-fucosidases of the GH29 and GH95 families from a fucoidan degrading cluster of the marine bacterium Wenyingzhuangia fucanilytica[J]. Archives of Biochemistry and Biophysics, 2022, 728: 109373. DOI:10.1016/j.abb.2022.109373.

[32]

THOGERSEN M S, CHRISTENSEN S J, JEPSEN M, et al. Transglycosylating β-D-galactosidase and α-L-fucosidase from Paenibacillus sp. 3179 from a hot spring in East Greenland[J]. Microbiologyopen, 2020, 9(3): e980. DOI:10.1002/mbo3.980.

[33]

LI Q, JIANG C F, TAN H D, et al. Characterization of recombinant E. coli expressing a novel fucosidase from Bacillus cereus 2-8 belonging to GH95 family[J]. Protein Expression and Purification, 2021, 186: 105897. DOI:10.1016/j.pep.2021.105897.

[34]

CURIEL J A, PEIROTEN A, LANGA S, et al. Characterization and stabilization of the α-L-fucosidase set from Lacticaseibacillus rhamnosus INIA P603[J]. Applied Microbiology and Biotechnology, 2022, 106(24): 8067-8077. DOI:10.1007/s00253-022-12262-w.

[35]

ONO A, SUZUKI T, GOTOH S, et al. Structural investigation of α-L-fucosidase from the pancreas of Patiria pectinifera, based on molecular cloning[J]. Carbohydrate Research, 2019, 475: 27-33. DOI:10.1016/j.carres.2019.02.001.

[36]

WEGNER C E, RICHTER-HEITMANN T, KLINDWORTH A, et al. Expression of sulfatases in Rhodopirellula baltica and the diversity of sulfatases in the genus Rhodopirellula[J]. Marine Genomics, 2013, 9: 51-61. DOI:10.1016/j.margen.2012.12.001.

[37]

SILCHENKO A S, RASIN A B, ZUEVA A O, et al. Fucoidan sulfatases from marine bacterium Wenyingzhuangia fucanilytica CZ1127T[J]. Biomolecules, 2018, 8(4): 98. DOI:10.3390/biom8040098.

[38]

VAN VLIET D M, PALAKAWONG NA AYUDTHAYA S, DIOP S, et al. Anaerobic degradation of sulfated polysaccharides by two novel Kiritimatiellales strains isolated from Black Sea sediment[J]. Frontiers in Microbiology, 2019, 10: 253. DOI:10.3389/fmicb.2019.00253.

[39]

MIKKELSEN M D, CAO H T T, RORET T, et al. A novel thermostable prokaryotic fucoidan active sulfatase PsFucS1 with an unusual quaternary hexameric structure[J]. Scientific Reports, 2021, 11(1): 19523. DOI:10.1038/s41598-021-98588-3.

[40]

NAGAO T, ARAI Y, YAMAOKA M, et al. Identification and characterization of the fucoidanase gene from Luteolibacter algae H18[J]. Journal of Bioscience and Bioengineering, 2018, 126(5): 567-572. DOI:10.1016/j.jbiosc.2018.05.016.

[41]

QIU Y J, JIANG H, DONG Y Y, et al. Expression and biochemical characterization of a novel fucoidanase from Flavobacterium algicola with the principal product of fucoidan-derived disaccharide[J]. Foods, 2022, 11(7): 1025. DOI:10.3390/foods11071025.

[42]

SILCHENKO A S, KUSAYKIN M I, ZAKHARENKO A M, et al. Endo-1, 4-fucoidanase from Vietnamese marine mollusk Lambis sp. which producing sulphated fucooligosaccharides[J]. Journal of Molecular Catalysis B: Enzymatic, 2014, 102: 154-160. DOI:10.1016/j.molcatb.2014.02.007.

[43]

SAKAI T, KAWAI T, KATO I. Isolation and characterization of a fucoidan-degrading marine bacterial strain and its fucoidanase[J]. Marine Biotechnology, 2004, 6(4): 335-346. DOI:10.1007/s10126-003-0033-5.

[44]

SILCHENKO A S, USTYUZHANINA N E, KUSAYKIN M I, et al. Expression and biochemical characterization and substrate specificity of the fucoidanase from Formosa algae[J]. Glycobiology, 2017, 27(3): 254-263. DOI:10.1093/glycob/cww138.

[45]

GEORGE A, SHRIVASTAV P S. Fucoidan, a brown seaweed polysaccharide in nanodrug delivery[J]. Drug Delivery and Translational Research, 2023, 13(10): 2427-2446. DOI:10.1007/s13346-023-01329-4.

[46]

FURUKAWA S I, FUJIKAWA T, KOGA D, et al. Production of fucoidan-degrading enzymes, fucoidanase, and fucoidan sulfatase by Vibrio sp. N-5[J]. Nippon Suisan Gakkaish, 1992, 58(8): 1499-1503. DOI:10.2331/SUISAN.58.1499.

[47]

DONG S J, CHANG Y G, SHEN J J, et al. Purification, expression and characterization of a novel α-L-fucosidase from a marine bacteria Wenyingzhuangia fucanilytica[J]. Protein Expression and Purification, 2017, 129: 9-17. DOI:10.1016/j.pep.2016.08.016.

[48]

KOVAL’OVA T, KOVAL T, STRANSKY J, et al. The first structure-function study of GH151 α-L-fucosidase uncovers new oligomerization pattern, active site complementation, and selective substrate specificity[J]. The FEBS Journal, 2022, 289(16): 4998-5020. DOI:10.1111/febs.16387.

[49]

SILCHENKO A S, RASIN A B, ZUEVA A O, et al. Discovery of a fucoidan endo-4O-sulfatase: regioselective 4O-desulfation of fucoidans and its effect on anticancer activity in vitro[J]. Carbohydrate Polymers, 2021, 271: 118449. DOI:10.1016/j.carbpol.2021.118449.

[50]

SAKURAMA H, TSUTSUMI E, ASHIDA H, et al. Differences in the substrate specificities and active-site structures of two α-L-fucosidases (glycoside hydrolase family 29) from Bacteroides thetaiotaomicron[J]. Bioscience Biotechnology and Biochemistry, 2012, 76(5): 1022-1024. DOI:10.1271/bbb.111004.

[51]

GROOTAERT H, VAN LANDUYT L, HULPIAU P, et al. Functional exploration of the GH29 fucosidase family[J]. Glycobiology, 2020, 30(9): 735-745. DOI:10.1093/glycob/cwaa023.

[52]

SUMMERS E L, MOON C D, ATUA R, et al. The structure of a glycoside hydrolase 29 family member from a rumen bacterium reveals unique, dual carbohydrate-binding domains[J]. Acta Crystallographica Section F-Structural Biology Communications, 2016, 72: 750-761. DOI:10.1107/S2053230X16014072.

[53]

NAGAE M, TSUCHIYA A, KATAYAMA T, et al. Structural basis of the catalytic reaction mechanism of novel 1, 2-α-L-fucosidase from Bifidobacterium bifidum[J]. Journal of Biological Chemistry, 2007, 282(25): 18497-18509. DOI:10.1074/jbc.M702246200.

[54]

COLIN S, DENIAUD E, JAM M, et al. Cloning and biochemical characterization of the fucanase FcnA: definition of a novel glycoside hydrolase family specific for sulfated fucans[J]. Glycobiology, 2006, 16(11): 1021-1032. DOI:10.1093/glycob/cwl029.

[55]

VICKERS C, LIU F, ABE K, et al. Endo-fucoidan hydrolases from glycoside hydrolase family 107 (GH107) display structural and mechanistic similarities to α-L-fucosidases from GH29[J]. Journal of Biological Chemistry, 2018, 293(47): 18296-18308. DOI:10.1074/jbc.RA118.005134.

[56]

NDEH D, ROGOWSKI A, CARTMELL A, et al. Complex pectin metabolism by gut bacteria reveals novel catalytic functions[J]. Nature, 2017, 544(7648): 65-70. DOI:10.1038/nature21725.

[57]

SHEN J J, CHANG Y G, ZHANG Y Y, et al. Discovery and characterization of an endo-1, 3-fucanase from marine bacterium Wenyingzhuangia fucanilytica: a novel glycoside hydrolase family[J]. Frontiers in Microbiology, 2020, 11: 1674. DOI:10.3389/fmicb.2020.01674.

[58]

SELA D A, GARRIDO D, LERNO L, et al. Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides[J]. Applied and Environmental Microbiology, 2012, 78(3): 795-803. DOI:10.1128/aem.06762-11.

[59]

KLONTZ E H, LI C, KIHN K, et al. Structure and dynamics of an α-fucosidase reveal a mechanism for highly efficient IgG transfucosylation[J]. Nature Communications, 2020, 11(1): 6204. DOI:10.1038/s41467-020-20044-z.

[60]

HONG H, KIM D H, SEO H, et al. Dual alpha-1, 4-and beta-1, 4-glycosidase activities by the novel carbohydrate-binding module in α-L-fucosidase from Vibrio sp. strain EJY3[J]. Journal of Agricultural and Food Chemistry, 2021, 69(11): 3380-3389. DOI:10.1021/acs.jafc.0c08199.

[61]

VIEIRA P S, BONFIM I M, ARAUJO E A, et al. Xyloglucan processing machinery in Xanthomonas pathogens and its role in the transcriptional activation of virulence factors[J]. Nature Communications, 2021, 12(1): 4049. DOI:10.1038/s41467-021-24277-4.

[62]

HETTLE A G, VICKERS C J, BORASTON A B. Sulfatases: critical enzymes for algal polysaccharide processing[J]. Frontiers in Plant Science, 2022, 13: 837636. DOI:10.3389/fpls.2022.837636.

[63]

SILCHENKO A S, RASIN A B, KUSAYKIN M I, et al. Structure, enzymatic transformation, anticancer activity of fucoidan and sulphated fucooligosaccharides from Sargassum horneri[J]. Carbohydrate Polymers, 2017, 175: 654-660. DOI:10.1016/j.carbpol.2017.08.043.

[64]

SILCHENKO A S, RASIN A B, KUSAYKIN M I, et al. Modification of native fucoidan from Fucus evanescens by recombinant fucoidanase from marine bacteria Formosa algae[J]. Carbohydrate Polymers, 2018, 193: 189-195. DOI:10.1016/j.carbpol.2018.03.094.

[65]

XU Z G, ZUO Z Q, GAOWA B, et al. The antithrombotic effects of low molecular weight fragment from enzymatically modified of Laminaria japonica polysaccharide[J]. Medical Science Monitor, 2020, 26: e920221. DOI:10.12659/MSM.920221.

[66]

WAN L, ZHU Y Y, ZHANG W L, et al. α-L-Fucosidases and their applications for the production of fucosylated human milk oligosaccharides[J]. Applied Microbiology and Biotechnology, 2020, 104(13): 5619-5631. DOI:10.1007/s00253-020-10635-7.

[67]

REBELLO O D, NICOLARDI S, LAGEVEEN-KAMMEIJER G S M, et al. A matrix-assisted laser desorption/ionization-mass spectrometry assay for the relative quantitation of antennary fucosylated N-glycans in human plasma[J]. Frontiers in Chemistry, 2020, 8: 138. DOI:10.3389/fchem.2020.00138.

[68]

DEMUS D, JANSEN B C, GARDNER R A, et al. Interlaboratory evaluation of plasma N-glycan antennary fucosylation as a clinical biomarker for HNF1A-MODY using liquid chromatography methods[J]. Glycoconjugate Journal, 2021, 38(3): 375-386. DOI:10.1007/s10719-021-09992-w.

[69]

MANIVASAGAN P, OH J. Production of a novel fucoidanase for the green synthesis of gold nanoparticles by Streptomyces sp. and its cytotoxic effect on HeLa cells[J]. Marine Drugs, 2015, 13(11): 6818-6837. DOI:10.3390/md13116818.

[70]

OHMES J, MIKKELSEN M D, NGUYEN T T, et al. Depolymerization of fucoidan with endo-fucoidanase changes bioactivity in processes relevant for bone regeneration[J]. Carbohydrate Polymers, 2022, 286: 119286. DOI:10.1016/j.carbpol.2022.119286.

Food Science
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Cite this article:
WEI Z, CHEN J, YANG J. Research Progress on Fucoidan-Degrading Enzymes. Food Science, 2024, 45(9): 306-313. https://doi.org/10.7506/spkx1002-6630-20230512-103
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