Insight into carrageenases: major review of sources, category, property, purification method, structure, and applications

References

• Campo VL, Kawano DF, Silva Júnior DBD, et al. Carrageenans: biological properties, chemical modifications and structural analysis - a review. Carbohyd Polym. 2009;77:167–180.
   Web of Science ®Google Scholar
• Usov AI. Structural analysis of red seaweed galactans of agar and carrageenan groups. Food Hydrocolloids. 1998;12:301–308.
   Web of Science ®Google Scholar
• Aliste AJ, Vieira FF, Mastro NLD. Radiation effects on agar, alginates and carrageenan to be used as food additives. Radiat Physics Chem. 2000;57:305–308.
   Web of Science ®Google Scholar
• Weiner ML. Food additive carrageenan: part II: a critical review of carrageenan in vivo safety studies. Crit Rev Toxicol. 2014;44:244–269.
   PubMed Web of Science ®Google Scholar
• Bonnaud M, Weiss J, Mcclements DJ. Interaction of a food-grade cationic surfactant (Lauric arginate) with food-grade biopolymers (pectin, carrageenan, xanthan, alginate, dextran, and chitosan). J Agric Food Chem. 2010;58:9770–9777.
   PubMed Web of Science ®Google Scholar
• Yu G, Guan H, Ioanoviciu AS, et al. Structural studies on kappa-carrageenan derived oligosaccharides. Carbohydr Res. 2002;337:433–440.
   PubMed Web of Science ®Google Scholar
• Arfors KE, Ley K. Sulfated polysaccharides in inflammation. J Lab Clin Med. 1993;121:201–202.
   PubMed Web of Science ®Google Scholar
• Yao Z, Wu H, Zhang S, et al. Enzymatic preparation of κ-carrageenan oligosaccharides and their anti-angiogenic activity. Carbohyd Polym. 2014;101:359–367.
   PubMed Web of Science ®Google Scholar
• Suzuki N, Kitazato K, Takamatsu J, et al. Antithrombotic and anticoagulant activity of depolymerized fragment of the glycosaminoglycan extracted from Stichopus japonicus Selenka. Thromb Haemost. 1991;65:369–373.
   PubMed Web of Science ®Google Scholar
• Hu X, Jiang X, Aubree E, et al. Preparation and in vivo. Antitumor activity of κ-carrageenan oligosaccharides. Pharm Biol. 2006;44:646–650.
   Web of Science ®Google Scholar
• Trincone A. Short bioactive marine oligosaccharides: diving into recent literature. Curr Biotechnol. 2015;4:212–222.
   Google Scholar
• Sun T, Tao H, Zhou D, et al. The effects of different degradation methods on antioxidant activities of κ-carrageenan oligosaccharides. Food Ferment Ind. 2009;24–27.
   Google Scholar
• Yuan H, Li N, Gao X, et al. Preparation and in vitro antioxidant activity of kappa-carrageenan oligosaccharides and their oversulfated, acetylated, and phosphorylated derivatives. Carbohydr Res. 2005;340:685–692.
   PubMed Web of Science ®Google Scholar
• Mou H, Jiang X, Guan H. A κ-carrageenan derived oligosaccharide prepared by enzymatic degradation containing anti-tumor activity. J Appl Phycol. 2003;15:297–303.
   Web of Science ®Google Scholar
• Michel G, Nyvalcollen P, Barbeyron T, et al. Bioconversion of red seaweed galactans: a focus on bacterial agarases and carrageenases. Appl Microbiol Biotechnol. 2006;71:23–33.
   PubMed Web of Science ®Google Scholar
• Mchugh DJ. Production and utilization of products from commercial seaweeds. J Bacteriol. 1987;176:460–468.
   Google Scholar
• Knutsen SH, Grasdalen H. Analysis of carrageenans by enzymic degradation, gel filtration and 1 H NMR spectroscopy. Carbohyd Polym. 1992;19:199–210.
   Web of Science ®Google Scholar
• Funami T, Hiroe M, Noda S, et al. Influence of molecular structure imaged with atomic force microscopy on the rheological behavior of carrageenan aqueous systems in the presence or absence of cations. Food Hydrocolloid. 2007;21:617–629.
   Web of Science ®Google Scholar
• Liu L. Influence of microwave irradiation on properties of carrageenan. Guangdong Chem Ind. 2003;16–19.
   Google Scholar
• Zhou YJ, Zhang YC, Zhang DL, et al. Ultrasonic assisted extraction of alkali treatment effect on carrageenan. Food Sci Tech. 2016;41:91–94.
   Google Scholar
• Zhou GF, Sun YP, Xin H, et al. In vivo antitumor and immunomodulation activities of different molecular weight Lambda-Carrageenans from Chondrus ocellatus. Pharmacol Res. 2004;50:47–53.
   PubMed Web of Science ®Google Scholar
• Cáceres PJ, Carlucci MJ, Damonte EB, et al. Carrageenans from Chilean samples of Stenogramme interrupta (Phyllophoraceae): structural analysis and biological activity. Phytochemistry. 2000;53:81–86.
   PubMed Web of Science ®Google Scholar
• Panlasigui LN, Baello OQ, Dimatangal JM, et al. Blood cholesterol and lipid-lowering effects of carrageenan on human volunteers. Asia Pac J Clin Nutr. 2003;12:209–214.
   PubMed Web of Science ®Google Scholar
• Skea GL, Mountfort DO, Clements KD. Contrasting digestive strategies in four New Zealand herbivorous fishes as reflected by carbohydrase activity profiles. Comp Biochem Phys A. 2007;146:63–70.
   PubMed Web of Science ®Google Scholar
• Mori T. On a carbohydrase acting on the mucilage from chondrus ocellatus holmes (I). Nippon Nōgeikagaku Kaishi. 1939;15:1070–1074.
   Google Scholar
• Greer CW, Yaphe W. Enzymatic analysis of carrageenans: structure of carrageenan from Eucheuma nudum. Hydrobiologia. 1984;116–117:563–567.
   Web of Science ®Google Scholar
• Gauthier G, Gauthier M, Christen R. Phylogenetic analysis of the genera Alteromonas, Shewanella, and Moritella using genes coding for small-subunit rRNA sequences and division of the genus Alteromonas into two genera, Alteromonas (emended) and Pseudoalteromonas gen. nov., and proposal of twe. Int J Syst Bacteriol. 1995;45:755–761.
   PubMedGoogle Scholar
• Jouanneau D, Boulenguer P, Mazoyer J, et al. Enzymatic degradation of hybrid iota-/nu-carrageenan by Alteromonas fortis iota-carrageenase. Carbohydr Res. 2010;345:934–940.
   PubMed Web of Science ®Google Scholar
• Xiaoyan XU, Shangyong LI, Yang X, et al. Cloning and characterization of a new κ-carrageenase gene from marine bacterium pseudoalteromonas sp. QY203. J Ocean Univ China. 2015;14:1082–1086.
   Web of Science ®Google Scholar
• Li S, Jia P, Wang L, et al. Purification and characterization of a new thermostable κ-carrageenase from the marine bacterium Pseudoalteromonas sp. QY203. J Ocean Univ China. 2013;12:155–159.
   Web of Science ®Google Scholar
• Duan GF, Bei SU, Han F, et al. Purification and characterization of a κ-carrageenase from marine pseudoalteromonas sp. QY202. J Ocean U China. 2010;40:95–100.
   Google Scholar
• Ziayoddin M, Lalitha J, Shinde M. Increased production of carrageenase by Pseudomonas aeruginosa ZSL-2 using Taguchi experimental design. Int Lett Nat Sci. 2014;17:194–207.
   Google Scholar
• Ohta Y, Hatada Y. A novel enzyme, lambda-carrageenase, isolated from a deep-sea bacterium. J Biochem. 2006;140:475–481.
   PubMed Web of Science ®Google Scholar
• Weigl J, Yaphe W. The enzymic hydrolysis of carrageenan by Pseudomonas carrageenovora: purification of a kappa-carrageenase. Can J Microbiol. 2011;12:939–947.
   Google Scholar
• Khambhaty Y, Mody K, Jha B. Purification and characterization of κ-carrageenase from a novel γ-proteobacterium, Pseudomonas elongata (MTCC 5261) syn. Microbulbifer elongatus comb. Biotechnol Bioprocess Eng. 2007;12:668–675.
   Web of Science ®Google Scholar
• Liu GL, Li Y, Chi Z, et al. Purification and characterization of κ-carrageenase from the marine bacterium Pseudoalteromonas porphyrae for hydrolysis of κ-carrageenan. Process Biochem. 2011;46:265–271.
   Web of Science ®Google Scholar
• Zhou MH, Ma JS, Li J, et al. A κ-carrageenase from a newly isolated pseudoalteromonas-like bacterium, WZUC10. Biotechnol Bioproc E. 2008;13:545–551.
   Web of Science ®Google Scholar
• Mclean MW, Williamson FB. kappa-Carrageenase from Pseudomonas carrageenovora. Eur J Biochem. 1979;93:553–558.
   PubMedGoogle Scholar
• Ma YX, Dong SL, Jiang XL, et al. Purification and characterization of κ-carrageenase from marine bacterium mutant strain pseudoalteromonas sp. Aj5-13 and its degraded products. J Food Biochem. 2010;34:661–678.
   Web of Science ®Google Scholar
• Kobayashi T, Uchimura K, Koide O, et al. Genetic and biochemical characterization of the Pseudoalteromonas tetraodonis alkaline κ-carrageenase. Biosci Biotech Biochem. 2012;76:506–511.
   PubMed Web of Science ®Google Scholar
• Feixue S, Yuexin M, Ying W, et al. Purification and characterization of novel κ-carrageenase from marine Tamlana sp. HC4. Chin J Oceanol Limn. 2010;28:1139–1145.
   Web of Science ®Google Scholar
• Yamaguchi K, Araki T, Aoki T, et al. Algal cell wall-degrading enzymes from viscera of marine animals. Nihon Suisan Gakkai Shi. 1989;55:105–110.
   Web of Science ®Google Scholar
• Zhu B, Ning L. Purification and characterization of a new κ-carrageenase from the marine bacterium Vibrio sp. NJ-2. J Microbiol Biotechnol. 2015;26:255–262.
   Web of Science ®Google Scholar
• Sun Y, Liu Y, Jiang K, et al. Electrospray ionization mass spectrometric analysis of κ-carrageenan oligosaccharides obtained by degradation with κ-carrageenase from Pedobacter hainanensis. J Agric Food Chem. 2014;62:2398–2405.
   PubMed Web of Science ®Google Scholar
• Wang L, Li S, Zhang S, et al. A new κ-carrageenase CgkS from marine bacterium Shewanella sp. Kz7. J Ocean Univ China. 2015;14:759–763.
   Web of Science ®Google Scholar
• Michel G, Labourel A, Thomas F, editors, et al. Treasure hunting in the genome of the marine bacterium Zobellia galactanivorans: discovery of novel enzymes for the bioconversion of algal polysaccharides. Polymerix. 2012;322–323.
   Google Scholar
• Thomas F, Bordron P, Eveillard D, et al. Gene expression analysis of zobellia galactanivorans during the degradation of algal polysaccharides reveals both substrate-specific and shared transcriptome-wide responses. Front Microbiol. 2017;8:1808–1821.
   PubMed Web of Science ®Google Scholar
• Matard-Mann M, Bernard T, Leroux C, et al. Structural insights into marine carbohydrate degradation by family GH16 kappa-carrageenases. J Biol Chem. 2017;292:19919–19934.
   PubMed Web of Science ®Google Scholar
• Yao Z, Wang F, Gao Z, et al. Characterization of a κ-carrageenase from marine Cellulophaga lytica strain N5-2 and analysis of its degradation products. Int J Mol Sci. 2013;14:24592–24602.
   PubMed Web of Science ®Google Scholar
• Cui H, Peng Y, Zhao B, et al. Cloning, identification and characterization of a novel κ-carrageenase from marine bacterium Cellulophaga lytica strain N5-2. Int J Biol Macromol. 2017;105:505–519.
   Web of Science ®Google Scholar
• Mou H, Jiang X, Liu Z, et al. Structural analysis of kappa-carrageenan oligosaccharides released by carrageenase from marine cytophaga mca-2. J Food Biochemistry. 2010;28:245–260.
   Google Scholar
• Sarwar G, Matayoshi S, Oda H. Purification of a kappa-carrageenase from marine Cytophaga species. Microbiol Immunol. 1987;31:869–877.
   PubMed Web of Science ®Google Scholar
• Kang S, Kim JK. Reuse of red seaweed waste by a novel bacterium, Bacillus sp. SYR4 isolated from a sandbar. World J Microbiol Biotechnol. 2015;31:209–217.
   PubMed Web of Science ®Google Scholar
• Youssef AS, Beltagy EA, El-Shenawy MA, et al. Production of k-carrageenase by Cellulosimicrobium cellulans isolated from Egyptian Mediterranean coast. Afr J Microbiol Res. 2012;6:6618–6628.
   Google Scholar
• Beltagy EA, Youssef AS, El-Shenawy MA, et al. Purification of kappa (k)-carrageenase from locally isolated Cellulosimicrobium cellulans. Afr J Microbiol Res. 2012;11:11438–11446.
   Google Scholar
• Su M, Duan G, Chai W, et al. Purification, cloning, characterization and essential amino acid residues analysis of a new κ-carrageenase from cellulophaga sp. QY3. PLoS One. 2013;8:1–11.
   Web of Science ®Google Scholar
• Ma S, Tan YL, Yu WG, et al. Cloning, expression and characterization of a new ι-carrageenase from marine bacterium, Cellulophaga sp. Biotechnol Lett. 2013;35:1617–1622.
   PubMed Web of Science ®Google Scholar
• Hatada Y, Mizuno M, Li Z, et al. Hyper-production and characterization of the ι-carrageenase useful for ι-carrageenan oligosaccharide production from a deep-sea bacterium, microbulbifer thermotolerans JAMB-A94 T, and Insight into the unusual catalytic mechanism. Mar Biotechnol. 2011;13:411–422.
   PubMed Web of Science ®Google Scholar
• Li S, Hao J, Sun M. Cloning and characterization of a new cold-adapted and thermo-tolerant ι-carrageenase from marine bacterium Flavobacterium sp. YS-80-122. Int J Biol Macromol. 2017;102:1059–1065.
   PubMed Web of Science ®Google Scholar
• Shen J, Chang Y, Dong S, et al. Cloning, expression and characterization of a ι-carrageenase from marine bacterium Wenyingzhuangia fucanilytica: a biocatalyst for producing ι-carrageenan oligosaccharides. J Biotechnol. 2017;259:103–109.
   PubMed Web of Science ®Google Scholar
• Michel G, Chantalat L, Fanchon E, et al. The iota-carrageenase of Alteromonas fortis. A beta-helix fold-containing enzyme for the degradation of a highly polyanionic polysaccharide. J Biol Chem. 2001;276:40202–40209.
   PubMed Web of Science ®Google Scholar
• Guibet M, Colin S, Barbeyron T, et al. Degradation of lambda-carrageenan by Pseudoalteromonas carrageenovora lambda-carrageenase: a new family of glycoside hydrolases unrelated to kappa- and iota-carrageenases. Biochem J. 2007;404:105–114.
   PubMed Web of Science ®Google Scholar
• Li J, Hu Q, Seswitazilda D. Purification and characterization of a thermostable λ-carrageenase from a hot spring bacterium, Bacillus sp. Biotechnol Lett. 2014;36:1669–1674.
   PubMed Web of Science ®Google Scholar
• Barbeyron T, Flament D, Michel G, et al. The sulphated-galactan hydrolases, agarases and carrageenases: structural biology and molecular evolution. Cahiers De Biologie Marine. 2001;42:169–183.
   Web of Science ®Google Scholar
• Michel G, Chantalat L, Duee E, et al. The kappa-carrageenase of P. carrageenovora features a tunnel-shaped active site: a novel insight in the evolution of Clan-B glycoside hydrolases. Structure. 2001;9:513–525.
   PubMed Web of Science ®Google Scholar
• Barbeyron T, Michel G, Potin P, et al. iota-Carrageenases constitute a novel family of glycoside hydrolases, unrelated to that of kappa-carrageenases. J Biol Chem. 2000;275:35499–35505.
   PubMed Web of Science ®Google Scholar
• Henrissat B, Bairoch A. Updating the sequence-based classification of glycosyl hydrolases. Biochem J. 1996;316: 695–696.
   PubMed Web of Science ®Google Scholar
• Xiao A, Xu C, Lin Y, et al. Preparation and characterization of κ-carrageenase immobilized onto magnetic iron oxide nanoparticles. Electron J Biotechn. 2016;19:1–7.
   Web of Science ®Google Scholar
• Liu Z, Li G, Mo Z, et al. Molecular cloning, characterization, and heterologous expression of a new κ-carrageenase gene from marine bacterium Zobellia sp. ZM-2. Appl Microbiol Biotechnol. 2013;97:10057–10067.
   PubMed Web of Science ®Google Scholar
• Dyrset N, Lystad KQ, Levine DW. Development of a fermentation process for production of a κ-carrageenase from Pseudomonas carrageenovora. Enzyme Microb Tech. 1997;20:418–423.
   Web of Science ®Google Scholar
• Khambhaty Y, Mody K, Jha B, et al. Statistical optimization of medium components for κ-carrageenase production by Pseudomonas elongata. Enzyme Microb Tech. 2007;40:813–822.
   Web of Science ®Google Scholar
• Guo J, Zhang L, Lu X, et al. Medium optimization and fermentation kinetics for κ-carrageenase production by Thalassospira sp. Fjfst-332. Molecules. 2016;21:1479–1496.
   Web of Science ®Google Scholar
• Guo J, Zheng Z, Chen C, et al. Enhanced production of κ-carrageenase and κ-carrageenan oligosaccharides through immobilization of thalassospira sp. Fjfst-332 with magnetic Fe3O4-chitosan microspheres. J Agric Food Chem. 2017;65:7934–7943.
   PubMed Web of Science ®Google Scholar
• Liu Z, Lin T, Chen Y, et al. Efficient extracellular production of κ-carrageenase in Escherichia coli: effects of wild-type signal sequence and process conditions on extracellular secretion. J Biotechnol. 2014;185:8–14.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Chi Z, Xu Y, et al. High-level extracellular expression of κ-carrageenase in Brevibacillus choshinensis for the production of a series of κ-carrageenan oligosaccharides. Process Biochem. 2017;64:83–92.
   Web of Science ®Google Scholar
• Yu Y, Liu Z, Yang M, et al. Characterization of full-length and truncated recombinant κ-carrageenase expressed in Pichia pastoris. Front Microbiol. 2017;8:1544–1556.
   PubMed Web of Science ®Google Scholar
• Xu C, Lin Y, Ni H, et al. Characterization of immobilized carrageenase on superparamagnetic nanoparticles for oligosaccharide preparation. Nanosci Nanotechnol Lett. 2015;7:855–860.
   Google Scholar
• Zhu B, Ni F, Ning L, et al. Cloning and biochemical characterization of a novel κ-carrageenase from newly isolated marine bacterium Pedobacter hainanensis NJ-02. Int J Biol Macromol. 2017;108:1331–1338.
   PubMed Web of Science ®Google Scholar
• Kobayashi T, Koide O, Mori K, et al. Phylogenetic and enzymatic diversity of deep subseafloor aerobic microorganisms in organics- and methane-rich sediments off Shimokita Peninsula. Extremophiles. 2008;12:519–527.
   PubMed Web of Science ®Google Scholar
• Smith J, Mountfort D, Falshaw R. A zymogram method for detecting carrageenase activity. Anal Biochem. 2005;347:336–338.
   PubMed Web of Science ®Google Scholar
• Miller GL. Use of dinitrosalycylic acid as reagent for the determination of reducing sugars. Anal Chem. 1959;31:426–428.
   Web of Science ®Google Scholar
• Østgaard K, Wangen BF, Knutsen SH, et al. Large-scale production and purification of κ-carrageenase from Pseudomonas carrageenovora for applications in seaweed biotechnology. Enzyme Microb Tech. 1993;15:326–333.
   Web of Science ®Google Scholar
• Yuan H, Song J. Preparation, structural characterization and in vitro antitumor activity of kappa-carrageenan oligosaccharide fraction from Kappaphycus striatum. J Appl Phycol. 2005;17:7–13.
   Web of Science ®Google Scholar
• Sun Y, Yang B, Wu Y, et al. Structural characterization and antioxidant activities of κ-carrageenan oligosaccharides degraded by different methods. Food Chem. 2015;178:311–318.
   PubMed Web of Science ®Google Scholar
• Wang W, Zhang P, Hao C, et al. In vitro inhibitory effect of carrageenan oligosaccharide on influenza A H1N1 virus. Antiviral Res. 2011;92:237–246.
   PubMed Web of Science ®Google Scholar
• Pérez-Riverol A, Ramos AP, Díaz LFM, et al. In vitro antiviral activity of aqueous extract from red seaweed tricleocarpa fragilis to influenza a virus. Revista Cubana Farmacia. 2014;48:316–328.
   Google Scholar
• Yuan H, Song J, Li X, et al. Enhanced immunostimulatory and antitumor activity of different derivatives of κ-carrageenan oligosaccharides from Kappaphycus striatum. J Appl Phycol. 2011;23:59–65.
   Web of Science ®Google Scholar
• Thomson AW, Fowler EF. Carrageenan: a review of its effects on the immune system. Agents Actions. 1981;11:265–273.
   PubMedGoogle Scholar
• Zablackis E, Vreeland V, Kloareg B. Isolation of protoplasts from kappaphycus alvarezii var. tambalang (Rhodophyta) and Secretion of ι-carrageenan fragments by cultured cells. J Exp Bot. 1993;44:1515–1522.
   Web of Science ®Google Scholar
• Gross W. Preparation of protoplasts from the carrageenophyte Gigartina corymbifera (Kütz.) J. Ag. (Rhodophyta). J Microbiol Meth. 1990;12:217–223.
   Web of Science ®Google Scholar
• Gall YL, Braud JP, Kloareg B. Protoplast production in Chondrus crispus gametophytes (gigartinales, rhodophyta). Plant Cell Rep. 1990;8:582–585.
   PubMed Web of Science ®Google Scholar
• Anastyuk SD, Barabanova AO, Correc G, et al. Analysis of structural heterogeneity of κ/β-carrageenan oligosaccharides from Tichocarpus crinitus by negative-ion ESI and tandem MALDI mass spectrometry. Carbohyd Polym. 2011;86:546–554.
   Web of Science ®Google Scholar
• Guibet M, Kervarec N, Génicot S, et al. Complete assignment of 1 H and 13 C NMR spectra of Gigartina skottsbergii λ-carrageenan using carrabiose oligosaccharides prepared by enzymatic hydrolysis. Carbohyd Res. 2006;341:1859–1869.
   PubMed Web of Science ®Google Scholar
• Antonopoulos A, Favetta P, Lafosse M, et al. Characterisation of iota-carrageenans oligosaccharides with high-performance liquid chromatography coupled with evaporative light scattering detection. J Chromatogr A. 2004;1059:83–87.
   PubMed Web of Science ®Google Scholar
• Pedersen G, Hagen HA, Asferg L, et al., inventor; Novo Nordisk, assignee. Removal of printing paste thickener and excess dye after textile printing. United States patent US 5,405,414A. 1995.
   Google Scholar
• Kang DH, You SK, Joo YC, et al. Synergistic effect of the enzyme complexes comprising agarase, carrageenase and neoagarobiose hydrolase on degradation of the red algae. Bioresour Technol. 2018;250:666–672.
   PubMed Web of Science ®Google Scholar
• Calteau A, Jeudy A, Préchoux A, et al. Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria. Nat Commun. 2017;8:1685.
   PubMed Web of Science ®Google Scholar
• Chauhan PS, Saxena A. Bacterial carrageenases: an overview of production and biotechnological applications. Biotech. 2016;6:1–18.
   Google Scholar
• Martin M, Portetelle D, Michel G, et al. Microorganisms living on macroalgae: diversity, interactions, and biotechnological applications. Appl Microbiol Biotechnol. 2014;98:2917–2935.
   PubMed Web of Science ®Google Scholar
• Arnosti C. Microbial extracellular enzymes and the marine carbon cycle. Annu Rev Mar Sci. 2011;3:401–425.
   PubMed Web of Science ®Google Scholar
• Swain MR, Natarajan V, Krishnan C. Marine enzymes and microorganisms for bioethanol production. Adv Food Nutr Res. 2017;80:181.
   PubMedGoogle Scholar
• Imran M, Poduval PB, Ghadi SC. Bacterial degradation of algal polysaccharides in marine ecosystem. Singapore: Springer; 2017.
   Google Scholar