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Phytochemistry Reviews

, Volume 17, Issue 3, pp 535–571 | Cite as

Carrageenans and carrageenases: versatile polysaccharides and promising marine enzymes

  • Mehri Ghanbarzadeh
  • Asma Golmoradizadeh
  • Ahmad Homaei
Article

Abstract

Carrageenans are sulfated polysaccharides isolated from marine red algae that share a common backbone of D-galactose alternately linked by α(1,3) and β(1,4) glycosidic linkages. They are classified based on the number and the position of the sulfate ester groups and the occurrence of a 3,6 anhydro-ring in the α-linked galactose. Accordingly the three most commercially exploited carrageenans are κ-, ι-, and λ-carrageenans. Because of their biocompatibility, exceptional physicochemical features and emulsifying, thickening, gelling and stabilizing abilities, they have found several industrial application, especially in food, pharmaceutical and cosmetic industries. Moreover, carrageenans can be degraded into lower molecular weight oligosaccharides, which have been reported to have promising pharmacological properties and potential therapeutic applications. Enzymes which degrade carrageenans are called carrageenases and are produced only by marine bacterial species. These enzymes all are endohydrolases that hydrolyze the internal β 1,4 linkages in carrageenans and produce a series of homologous even-numbered oligosaccharides with various biological and physiological activities including anti-tumor, anti-inflammation, anti-viral, anti-coagulation, etc. Carrageenase enzymes have also other applications related to the biomedical field, bioethanol production, prevention of red algal bloom, obtaining algal protoplasts, etc. In the first part of this review, general information regarding structure, physicochemical properties, biological activities and potential applications of carrageenans is summarized. The second part deals with research and development works on some aspects of carrageenase enzymes like the source, characterization, the kinetics and biochemical properties and their applications in various industries.

Keywords

Carrageenan Carrageenan-degrading enzymes Bacterial carrageenases Biochemical properties Industrial applications 

Notes

Acknowledgements

The authors express their gratitude to the research council of the University of Hormozgan for financial support during the course of this project.

References

  1. Abad LV, Kudo H, Saiki S, Nagasawa N, Tamada M, Katsumura Y et al (2009) Radiation degradation studies of carrageenans. Carbohydr Polym 78:100–106Google Scholar
  2. Abad LV, Kudo H, Saiki S, Nagasawa N, Tamada M, Fu H et al (2010) Radiolysis studies of aqueous κ-carrageenan. Nucl Instr Meth Phys Res B 268:1607–1612Google Scholar
  3. Abdul Khalil HPS, Saurabh CK, Tye YY et al (2017) Seaweed based sustainable films and composites for food and pharmaceutical applications: a review. Renew Sustain Energy Rev 77:353–362Google Scholar
  4. Abt B, Lu M, Misra M, Han C, Nolan M et al (2011) Complete genome sequence of Cellulophaga algicola type strain (IC166). Stand Genom Sci 4:72–80Google Scholar
  5. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169Google Scholar
  6. Araki T, Higashimoto Y, Morishita T (1999) Purification and characterization of κ-carrageenase from a marine bacterium, Vibrio sp. CA-1004. Fish Sci 65:937–942Google Scholar
  7. Arora D, Sharma N, Sharma V et al (2016) An update on polysaccharide-based nanomaterials for antimicrobial applications. Appl Microbiol Biotechnol 100:2603–2615Google Scholar
  8. Barbeyron T, Henrissat B, Kloareg B (1994) The gene encoding the κ-carrageenase of Alteromonas carrageenovora is related to β-1,3-1,4-glucanases. Gene 139:105–109Google Scholar
  9. Barbeyron T, Gerard A, Potin P, Henrissat B, Kloareg B (1998) The κ-carrageenase of the marine bacterium Cytophaga drobachiensis. Structural and phylogenetic relationships within family-16 glycoside hydrolases. Mol Biol Evol 15:528–537Google Scholar
  10. Barbeyron T, Michel G, Potin P, Henrissat B, Kloareg B (2000) Iota-carrageenases constitute a novel family of glycoside hydrolases, unrelated to that of kappa-carrageenases. J Biol Chem 275:35499–35505Google Scholar
  11. Barbeyron T, Brillet-Gueguen L, Carre W, Carrière C, Caron C, Czjzek M et al (2016) Matching the diversity of sulfated biomolecules: creation of a classification database for sulfatases reflecting their substrate specificity. PLoS ONE 11:e0164846Google Scholar
  12. Bellion C, Hamer GK, Yaphe W (1981) Analysis of kappaiota hybrid carrageenans with kappa-carrageenase, iotacarrageenase and 13C-NMR. Proc Int Seaweed Symp 10:379–384Google Scholar
  13. Bellion C, Hamar G, Yaphe W (1982) The degradation of Eucheuma spinosum and Eucheuma cottinii carrageenans by ι-carrageenases and κ carrageenases from marine bacteria. Can J Microbiol 28:874–884Google Scholar
  14. Beltagy EA, Youssef AS, El-Shenaway MA, El-Assar SA (2012) Purification of kappa (κ)-carrageenase from locally isolated Cellulosimicrobium cellulans. Afr J Biotechnol 11:11438–11446Google Scholar
  15. Beygmoradi A, Homaei A (2017) Marine Microbes as a valuable resource for brand new industrial biocatalysts. Biocatal Agric Biotechnol 11:131–152Google Scholar
  16. Bhardwaj TR, Kanwar M, Lal R, Gupta A (2000) Natural gums and modified natural gums as sustained-release carriers. Drug Dev Ind Pharm 26:1025–1038Google Scholar
  17. Bhattacharyya S, Borthakur A, Dudeja PK, Tobacman JK (2008) Carrageenan induces cell cycle arrest in human intestinal epithelial cells in vitro. J Nutr 138:469–475Google Scholar
  18. Bonferoni MC, Rossi S, Tamayo M, Pedraz JL, Dominguez-Gil A, Caramella C (1993) On the employment of λ-carrageenan in a matrix system. I. Sensitivityto dissolution medium and comparison with Na carboxymethylcellulose andxanthan gum. J Control Release 26:119–127Google Scholar
  19. Bonferoni MC, Rossi S, Tamayo M et al (1994) On the employment of λ-carrageenan in a matrix system. II. λ-Carrageenan and hydroxypropylmethylcellulose mixtures. J Control Release 30:175–182Google Scholar
  20. Bonferoni MC, Rossi S, Ferrari F, Caramella C (2004a) Development of oralcontrolled-release tablet formulations based on diltiazem-carrageenan complex. Pharm Dev Technol 9:155–162Google Scholar
  21. Bonferoni MC, Rossi S, Ferrari F, Caramella C (2004b) Development of oral controlled-release tablet formulations based on diltiazem-carrageenan complex. Pharm Dev Technol 9:155–162Google Scholar
  22. Briones AV, Sato T (2010) Encapsulation of glucose oxidase (GOD) in polyelectrolyte complexes of chitosan–carrageenan. React Function Polym 70:19–27Google Scholar
  23. Buck CB, Thompson CD, Roberts JN, Muller M, Lowy DR, Schiller JT (2006) Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathog 2:e69Google Scholar
  24. Bulmer C, Margaritis A, Xenocostas A (2012) Encapsulation and controlledrelease of recombinant human erythropoietin from chitosan–carrageenannanoparticles. Curr Drug Deliv 9:527–537Google Scholar
  25. Campo VL, Kawano DF, Silva JDB, Carvalho I (2009) Carrageenans: biological properties, chemical modifications and structural analysis—a review. Carbohydr Polym 77:167–180Google Scholar
  26. Cánovas M, Bernal V, González M et al (2005) Factors affecting the biotransformation of trimethylammonium compounds into l-carnitine by Escherichia coli. Biochem Eng J 26:145–154Google Scholar
  27. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V et al (2009) The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238Google Scholar
  28. Caram-Lelham N, Sundelöf LO (1996) The effect of hydrophobic character of drugs and helix-coil transition of kappa-carrageenan on the polyelectrolyte-drug interaction. Pharm Res 13:920–925Google Scholar
  29. Caram-Lelham N, Sundelöf LO, Andersson T (1995) Preparative separation of oligosaccharides from κ-carrageenan, sodium hyaluronate, and dextran by Superdex™ 30 prep. grad. Carbohydr Res 273:71–76Google Scholar
  30. Cardoso M, Costa R, Mano J (2016) Marine origin polysaccharides in drug delivery systems. Mar Drugs 14:34Google Scholar
  31. Chandrasekaran M, Kumar SR (2010) Marine microbial enzymes. In: Werner H, Roken S (eds) Biotechnology. EOLSS, Paris, pp 47–79Google Scholar
  32. Chauhan PS, Gupta N (2017) Insight into microbial mannosidases: a review. Crit Rev Biotechnol 37:190–201Google Scholar
  33. Chauhan PS, Saxena A (2016) Bacterial carrageenases: an overview of production and biotechnological applications. Biotech 6:1–18Google Scholar
  34. Chauhan PS, Puri N, Sharma P, Gupta N (2012) Mannanases: microbial sources, production, properties and potential biotechnological applications. Appl Microbiol Biotechnol 93:1817–1830Google Scholar
  35. Chauhan PS, Bharadwaj A, Puri N, Gupta N (2014a) Optimization of medium composition for alkali-thermostable mannanase production by Bacillus nealsonii PN-11 in submerged fermentation. Int J Curr Microbiol Appl Sci 3:1033–1045Google Scholar
  36. Chauhan PS, Sharma P, Puri N, Gupta N (2014b) A process for reduction in viscosity of coffee extract by enzymatic hydrolysis of mannan. Biosystems Eng 37:1459–1467Google Scholar
  37. Chauhan PS, Sharma P, Puri N, Gupta N, Res EF (2014c) Purification and characterization of an alkali-thermostable B-mannanase from Bacillus nealsonii PN-11 and its application in manno-oligosaccharides preparation having prebiotic potential. Eur Food Res Technol 238:927–936Google Scholar
  38. Chauhan PS, Soni SK, Sharma P, Saini A, Gupta N (2014d) A mannanase from Bacillus nealsonii PN-11: statistical optimization of production and application in biobleaching of pulp in combination with xylanase. Int J Pharma Bio Sci 5:237–251Google Scholar
  39. Chen LCM, Craigie JS, Xie ZK (1994) Protoplast production from Porphyra linearis using a simplified agarase procedure capable of commercial application. J Appl Phys 6:35–39Google Scholar
  40. Chen HM, Yan XJ, Wang F, Xu WF, Zhang L (2010) Assessment of the oxidative cellular toxicity of a κ-carrageenan oxidative degradation product towards Caco-2 cells. Food Res Int 43:2390–2401Google Scholar
  41. Collén PN, Lemoine M, Daniellou R, Guégan J-P, Paoletti S, Helbert W (2009) Enzymatic degradation of κ-carrageenan in aqueous solution. Biomacromol 10:1757–1767Google Scholar
  42. Copeland A, Lucas S, Lapidus A, Barry K, Detter JC, Glavina del Rio T et al (2006) Complete sequence of Pseudoalteromonas Atlantica T6c. US DOE Joint Genome Institute, Walnut CreekGoogle Scholar
  43. Craigie JS (1990) Cell walls. In: Cole K, Sheath R (eds) Biology of the red algae. Cambridge University Press, Cambridge, pp 221–257Google Scholar
  44. Cunha L, Grenha A (2016) Sulfated seaweed polysaccharides as multifunctional materials in drug delivery applications. Mar Drugs 14:42Google Scholar
  45. d’Ayala GG, Malinconico M, Laurienzo P (2008) marine derived polysaccharides for biomedical applications: chemical modification approaches. Molecules 13:2069–2106Google Scholar
  46. Dadshahi Z, Homaei A, Zeinali F, Sajedi RH, Khajeh K (2016) Extraction and purification of a highly thermostable alkaline caseinolytic protease from wastes Penaeus vannamei suitable for food and detergent industries. Food Chem 202:110–115Google Scholar
  47. Dafe A, Etemadi H, Zarredar H, Mahdavinia GR (2017) Development of novel carboxymethyl cellulose/k-carrageenan blends as an enteric delivery vehicle for probiotic bacteria. Int J Biol Macromol 97:299–307Google Scholar
  48. Daniel-da-Silva AL, Trindade T, Goodfellow BJ et al (2007) In situ synthesis of magnetite nanoparticles in carrageenan gels. Biomacromol 8:2350–2357Google Scholar
  49. Daniel-da-Silva AL, Lóio R, Lopes-da-Silva JA et al (2008) Effects of magnetite nanoparticles on the thermorheological properties of carrageenan hydrogels. J Colloid Interface Sci 324:205–211Google Scholar
  50. Daniel-da-Silva AL, Moreira J, Neto R, Estrada AC, Gil AM, Trindade T (2012) Impact of magnetic nanofillers in the swelling and release proper-ties of kappa-carrageenan hydrogel nanocomposites. Carbohydr Polym 87:328–335Google Scholar
  51. De Ruiter GA, Rudolph B (1997) Carrageenan biotechnology. Trends Food SciTechnol 8:389–395Google Scholar
  52. De SF-Tischera PC, Talarico L, Noseda M, Guimaraes SMP, Damonte E, Duarte M (2006) Chemical structure and antiviral activity of carrageenans from Meristiella gelidium against herpes simplex and dengue virus. Carbohydr Polym 63:459–465Google Scholar
  53. Debashish G, Malay S, Barindra S, Joydeep M (2005) Marine enzymes. Adv Biochem Eng/Biotechnol 96:189–218Google Scholar
  54. Decamps C, Norton S, Poncelet D, Neufeld RJ (2004) Continuous pilot plant–scale immobilization of yeast in κ-carrageenan gel beads. AIChE J 50:1599–1605Google Scholar
  55. Devi N, Maji TK (2010) Microencapsulation of isoniazid in genipin-crosslinked gelatin-A-κ-carrageenan polyelectrolyte complex. Drug Dev Ind Pharm 36:56–63Google Scholar
  56. Elnashar MMM, Wahba MI, Amin MA, Eldiwany AI (2014) Application of Plackett–Burman screening design to the modeling of grafted alginate–carrageenan beads for the immobilization of penicillin G acylase. J Appl Polym Sci 131:40285–40295Google Scholar
  57. Esawy MA, Awad GEA, Wahab WAA et al (2016) Immobilization of halophilic Aspergillus awamori EM66 exochitinase on grafted k-carrageenan-alginate beads. 3 Biotech 6:29Google Scholar
  58. Estrada AC, Daniel-da-Silva AL, Trindade T (2013) Photothermally enhanced drug release by [small kappa]-carrageenan hydrogels reinforced with multi-walled carbon nanotubes. RSC Adv 3:10828–10836Google Scholar
  59. Foley PM, Beach ES, Zimmerman JB (2011) Algae as a source of renewable chemicals: opportunities and challenges. Green Chem 13:1399Google Scholar
  60. Fu XT, Kim SM (2010) Agarase: review of major sources, categories, purification method, enzyme characteristics and applications. Mar Drugs 8:200–218Google Scholar
  61. Funami T, Hiroe M, Noda S et al (2007) 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 Hydrocoll 21:617–629Google Scholar
  62. Gasperini L, Mano JF, Reis RL (2014) Natural polymers for the microencapsulation of cells. J R Soc Interface 11:20140817Google Scholar
  63. Genicot SM, Groisillier A, Rogniaux H, Meslet-Cladière L, Barbeyron T, Helbert W (2014) Discovery of a novel iota carrageenan sulfatase isolated from the marine bacterium Pseudoalteromonas carrageenovora. Front Chem 2:2Google Scholar
  64. Girond S, Crance JM, Van Cuyck-Gandre H, Renaudet J, Deloince R (1991) Antiviral activity of carrageenan on hepatitis A virus replication in cell culture. Res Virol 142:261–270Google Scholar
  65. Glöckner FO, Kube M, Bauer M, Teeling H, Lombardot T, Ludwig W et al (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci 100:8298–8303Google Scholar
  66. Gonçalves VSS, Gurikov P, Poejo J et al (2016) Alginate-based hybrid aerogel microparticles for mucosal drug delivery. Eur J Pharm Biopharm 107:160–170Google Scholar
  67. Greer CW, Yaphe W (1984) Purification and properties of iotacarrageenase from a marine bacterium. Can J Microbiol 30:1500–1506Google Scholar
  68. Grenha A, Gomes ME, Rodrigues M, Santo VE, Mano JF, Neves NM, Reis RL (2010) Development of new chitosan/carrageenan nanoparticles for drug delivery applications. J Biomed MaterRes A 92:1265–1272Google Scholar
  69. Guibet M, Colin S, Barbeyron T, Genicot S, Kloareg B et al (2007) Degradation of lambda-carrageenan by Pseudoalteromonas carrageenovora lambda-carrageenase: a new family of glycoside hydrolases unrelated to kappa- and iotacarrageenases. Biochem J 404:105–114Google Scholar
  70. Guibet M, Boulenguer P, Mazoyer J et al (2008) Composition and distribution of carrabiose moieties in hybrid κ-/ι-carrageenans using carrageenases. Biomacromol 9:408–415Google Scholar
  71. Gurpilhares DdB, Moreira TR, Bueno JdL et al (2016) Algae’s sulfated polysaccharides modifications: potential use of microbial enzymes. Process Biochem 51:989–998Google Scholar
  72. Haijin M, Xiaolu J, Huashi G (2003) A κ-carrageenan derived oligosaccharide prepared by enzymatic degradation containing anti-tumor activity. J Appl Phys 15:297–303Google Scholar
  73. Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68(4):669–685Google Scholar
  74. Hariharan M, Wheatley TA, Price JC (1997) Controlled-release tablet matrices from carrageenans: compression and dissolution studies. Pharm Dev Technol 2:383–393Google Scholar
  75. Hatada Y, Mizuno M, Li Z, Ohta Y (2011) Hyper-production and characterization of the ι-carrageenase useful for ι-carrageenan oligosaccharide production from a deep-sea bacterium, Microbulbifer thermotolerans JAMB-A94T, and insight into the unusual catalytic mechanism. Mar Biotechnol 13:411–422Google Scholar
  76. Hawkes MW (1990) Reproductive strategies. In: Cole KM, Sheath RG (eds) Biology of the red algae. Press Syndicate of the University of Cambridge, New York, pp 455–476Google Scholar
  77. He Y-C, Xu J-H, Su J-H, Zhou L (2010) Bioproduction of glycolic acid from glycolonitrile with a new bacterial isolate of Alcaligenes sp. ECU0401. Appl Biochem Biotechnol 160:1428–1440Google Scholar
  78. Hebar A, Koller C, Seifert J-M et al (2015) Non-clinical safety evaluation of intranasal iota-carrageenan. PLoS ONE 10:e0122911Google Scholar
  79. Hehemann J-H, Boraston AB, Czjzek M (2014) A sweet new wave: structures and mechanisms of enzymes that digest polysaccharides from marine algae. Curr Opin Struct Biol 28:77–86Google Scholar
  80. Helbert W (2017) Marine polysaccharide sulfatases. Front Mar Sci 4:1–10Google Scholar
  81. Henares BM, Enriquez EP, Dayrit FM, Rojas NRL (2010) Iota-carrageenan hydrolysis by Pseudoalteromonas carrageenovora IFO12985. Philipp J Sci 139:131–138Google Scholar
  82. Hezaveh H, Muhamad II (2012) The effect of nanoparticles on gastrointestinalrelease from modified kappa-carrageenan nanocomposite hydrogels. Carbohydr Polym 89:138–145Google Scholar
  83. Hezaveh H, Muhamad II, Noshadi I, Shu Fen L, Ngadi N (2012) Swelling behaviour and controlled drug release from cross-linked kappa-carrageenan/NaCMC hydrogel by diffusion mechanism. J Microencapsul 29:68–379Google Scholar
  84. Ho C-L (2015) Phylogeny of algal sequences encoding carbohydrate sulfotransferase, formylglycine-dependent sulfatases, and putative sulfatase modifying factors. Front Plant Sci 6:1057Google Scholar
  85. Homaei A (2015) Purification and biochemical properties of highly efficient alkaline phosphatase from Fenneropenaeus merguiensis brain. J Mol Catal B Enzym 118:16–22Google Scholar
  86. Homaei A, Ghanbarzadeh M, Monsef F (2016a) Biochemical features and kinetic properties of α-amylases from marine organisms. Int J Biol Macromol 83:306–314Google Scholar
  87. Homaei A, Lavajoo F, Sariri R (2016b) Development of marine biotechnology as a resource for novel proteases and their role in modern biotechnology. Int J Biol Macromol 88:542–552Google Scholar
  88. Hu XK, Jiang XL, Aubree E, Boulenguer P, Critchley AT (2006) Preparation and in vivo antitumor activity of kappa-carrageenan oligosaccharides. Pharm Biol 44:646–650Google Scholar
  89. Ishikura M, Hagiwara K, Takishita K, Haga M, Iwai K, Maruyama T (2004) Isolation of new Symbiodinium strains from tridacnid giant clam (Tridacna crocea) and sea slug (Pteraeolidia ianthina) using culture medium containing giant clam tissue homogenate. Mar Biotechnol 6:378–385Google Scholar
  90. Iurciuc (Tincu) C-E, Savin A, Atanase LI et al (2017) Physico-chemical characteristics and fermentative activity of the hydrogel particles based on polysaccharides mixture with yeast cells immobilized, obtained by ionotropic gelation. Food Bioprod Process 104:104–123Google Scholar
  91. Jam M, Flament D, Allouch J, Potin P, Thion L, Kloareg B, Czjzek M, Helbert W, Michel G, Barbeyron T (2005) The endo-β-agarases AgaA and AgaB from the marine bacterium Zobellia galactanivorans: two paralogue enzymes with different molecular organizations and catalytic behaviours. Biochem J 385:703–713Google Scholar
  92. Jiang Y, Jiang Y-J, Zhang Y-F et al (2007) Biosilica-coated κ-carrageenan microspheres for yeast alcohol dehydrogenase encapsulation. J Biomater Sci Polym Ed 18:1517–1526Google Scholar
  93. Jiao G, Yu G, Zhang J, Ewart H (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9:196–223Google Scholar
  94. John RP, Anisha GS, Nampoothiri KM, Pandey A (2011) Micro and macroalgal biomass: a renewable source for bioethanol. Bioresour Technol 102:186–193Google Scholar
  95. Jong WS, Saurí A, Luirink J (2010) Extracellular production of recombinant proteins using bacterial autotransporters. Curr Opin Biotechnol 21:646–652Google Scholar
  96. Jouanneau D, Boulenguer P, Mazoyer J, Helbert W (2010) Enzymatic degradation of hybrid ι-/ν-carrageenan by Alteromonas fortis-carrageenase. Carbohydr Res 345:934–940Google Scholar
  97. Joye IJ, McClements DJ (2016) Biopolymer-based delivery systems: challenges and opportunities. Curr Top Med Chem 16:1026–1039Google Scholar
  98. Kalitnik AA, Barabanova AOB, Nagorskaya VP, Reunov AV, Glazunov VP, Solov’eva TF, Yermak IM (2013) Low molecular weight derivatives of different carrageenan types and their antiviral activity. J Appl Phycol 25:65–72Google Scholar
  99. Kalsoom Khan A, Saba AU, Nawazish S et al (2017) Carrageenan based bionanocomposites as drug delivery tool with special emphasis on the influence of ferromagnetic nanoparticles. Oxid Med Cell Longev 2017:1–13Google Scholar
  100. Kang S, Kim JK (2015) Reuse of seaweed waste by a novel bacterium, Bacillus sp. SYR4 isolated from a sandbar. World J Microbiol Biotechnol 31:209–217Google Scholar
  101. Kavitha Reddy GKM, Satla S, Gaikwad S (2011) Natural polysaccharides: versatile excipients for controlled drug delivery systems. Asian J Pharm Sci 6:275–286Google Scholar
  102. Kawata K, Hanawa T, Endo N et al (2012) Formulation study on retinoic acid gel composed of iota-carrageenan, polyethylene oxide and Emulgen® 408. Chem Pharm Bull (Tokyo) 60:825–830Google Scholar
  103. Kennedy J, Marchesi JR, Dobson ADW (2008) Marine metagenomics strategies for discovery of novel enzymes with biotechnological applications from marine ecosystems. Microb Cell Fact 7:27Google Scholar
  104. Kennedy J, O’Leary ND, Kiran GS, Morrissey JP, O’Gara F, Selvin J, Dobson ADW (2011) Functional metagenomic strategies for the discovery of novel enzymes and biosurfactants with biotechnological applications from marine ecosystems. J Appl Microbiol 111:787–799Google Scholar
  105. Khambhaty Y, Mody K, Jha B (2007a) Purification and characterization of κ-carrageenase from a novel γ-proteobacterium, Pseudomonas elongata (MTCC 5261) syn. Microbulbifer elongatus comb. Nov. Biotechnol Bioprocess Eng 12:668–675Google Scholar
  106. Khambhaty Y, Mody K, Jha B, Gohel V (2007b) Statistical optimization of medium components for κ-carrageenase production by Pseudomonas elongate. Enzyme Microb Technol 40:813–822Google Scholar
  107. Kilmarx PH, van de Wijgert JHHM, Chaikummao S et al (2006) Safety and acceptability of the candidate microbicide Carraguard in Thai Women: findings from a Phase II Clinical Trial. J Acquir Immune Defic Syndr 43:327–334Google Scholar
  108. Kloareg B, Quatrano RS (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Rev 26:259–315Google Scholar
  109. Knudsen NR, Ale MT, Meyer AS (2015) eaweed hydrocolloid production: an update on enzyme assisted extraction and modification technologies. Mar Drugs 13:3340–3359Google Scholar
  110. Knutsen S, Myslabodski B, Larsen B, Usov A (1994) A modified system of nomenclature for red algal galactans. Bot Mar 37:163–169Google Scholar
  111. Kobayashi T, Uchimura K, Osamu K, Deguchi S, Horikoshi K (2012) Genetic and biochemical characterization of the Pseudoalteromonas tetraodonis alkaline κ-carrageenase. Biosci Biotechnol Biochem 76:506–511Google Scholar
  112. Kojima H, Yoshihara K, Sawada T, Kondo H, Sako K (2008) Extended releaseof a large amount of highly water-soluble diltiazem hydrochloride by utiliz-ing counter polymer in polyethylene oxides (PEO)/polyethylene glycol (PEG)matrix tablets. Eur J Pharm Biopharm 70:556–562Google Scholar
  113. Koklukaya SZ, Sezer S, Aksoy S, Hasirci N (2016) Polyacrylamide-based semi-interpenetrating networks for entrapment of laccase and their use in azo dye decolorization. Biotechnol Appl Biochem 63:699–707Google Scholar
  114. Korenblum E, Valoni É, Penna M, Seldin L (2010) Bacterial diversity in water injection systems of Brazilian offshore oil platforms. Appl Microbiol Biotechnol 85:791–800Google Scholar
  115. Krishnan MS, Nghiem NP, Davison BH (1999) Ethanol production from corn starch in a fluidized-bed bioreactor. Appl Biochem Biotechnol 77–79:359–371Google Scholar
  116. Lai VMF, Wong PAL, Li CY (2000) Effects of cation properties on sol-gel transition and gel properties of κ-carrageenan. J Food Sci 65:1332–1337Google Scholar
  117. Le Gall Y, Braud JP, Kloareg B (1990) Protoplast production in Chondrus crispus gametophytes (Gigartinales, Rhodophyta). Plant Cell Rep 8:582–585Google Scholar
  118. Leibbrandt A, Meier C, König-Schuster M, Weinmüllner R, Kalthoff D, Pflugfelder B, Graf P, Frank-Gehrke B, Beer M, Fazekas T, Unger H, Prieschl-Grassauer E, Grassauer A (2010) Iota-carrageenan is a potent inhibitor of influenza A virus infection. PLoS ONE 5:e14320Google Scholar
  119. Lemoine M, Nyvall Collén P, Helbert W (2009) Physical state of κ-carrageenan modulates the mode of action of κ-carrageenase from Pseudoalteromonas carrageenovora. Biochem J 419:545–553Google Scholar
  120. Leone G, Consumi M, Pepi S et al (2016) New formulations to enhance lovastatin release from red yeast rice (RYR). J Drug Deliv Sci Technol 36:110–119Google Scholar
  121. Li B, Zaveri T, Ziegler GR, Hayes JE (2013a) User preferences in a carrageenan-based vaginal drug delivery system. PLoS ONE 8:e54975Google Scholar
  122. Li L, Wang L, Shao Y et al (2013b) Elucidation of release characteristics of highly soluble drug trimetazidine hydrochloride from chitosan-carrageenan matrix tablets. J Pharm Sci 102:2644–2654Google Scholar
  123. Li S, Jia P, Wang L, Yu W, Hang F (2013c) Purification and characterization of a new thermostable κ-carrageenase from the marine bacterium Pseudoalteromonas sp. QY203. J Ocean Univ China 12:155–159Google Scholar
  124. Li J, Hu Q, Seswita-Zilda D (2014a) Purification and characterization of a thermostable κ-carrageenase from a hot spring bacterium, Bacillus sp. Biotechnol Lett 36:1669–1674Google Scholar
  125. Li L, Ni R, Shao Y, Mao S (2014b) Carrageenan and its applications in drug delivery. Carbohydr Polym 103:1–11Google Scholar
  126. Li Y, Huang Z, Qiao L, Gao Y, Guan H, Hwang H, Aker WG, Wang P (2015) Purification and characterization of a novel enzyme produced by Catenovulum sp. LP and its application in the pretreatment to Ulva prolifera for bio-ethanol production. Process Biochem 50:799–806Google Scholar
  127. Li S, Hao J, Sun M (2017) 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 102:1059–1065Google Scholar
  128. Lii C, Chen C-H, Yeh A-I, Lai VM-F (1999) Preliminary study on the degradation kinetics of agarose and carrageenans by ultrasound. Food Hydrocoll 13:477–481Google Scholar
  129. Lin B, Lu G, Li S, Hu Z, Chen H (2012) Draft genome sequence of the novel agarolytic bacterium Aquimarina agarilytica ZC1. J Bacteriol 194:2769Google Scholar
  130. Ling G, Zhang T, Zhang P et al (2016) Nanostructured lipid–carrageenan hybrid carriers (NLCCs) for controlled delivery of mitoxantrone hydrochloride to enhance anticancer activity bypassing the BCRP-mediated efflux. Drug Dev Ind Pharm 42:1351–1359Google Scholar
  131. Liu Z, Huang H (2016) Preparation and characterization of cellulose composite hydrogels from tea residue and carbohydrate additives. Carbohydr Polym 147:226–233Google Scholar
  132. Liu J, Li L (2007) Diffusion of camptothecin immobilized with cationic surfactant into agarose hydrogel containing anionic carrageenan. J Biomed MaterRes A 83A:1103–1109Google Scholar
  133. Liu F, Yu B (2015) Efficient production of reuterin from glycerol by magnetically immobilized Lactobacillus reuteri. Appl Microbiol Biotechnol 99:4659–4666Google Scholar
  134. Liu Y, Zhu Y, Wei G, Lu W (2009) Effect of carrageenan on poloxamer-based in situ gel for vaginal use: improved in vitro and in vivo sustained-release properties. Eur J Pharm Sci 37:306–312Google Scholar
  135. Liu GL, Li Y, Chi Z, Chi ZM (2011a) Purification and characterization of κ-carrageenase from the marine bacterium Pseudoalteromonas porphyrae for hydrolysis of κ-carrageenan. Process Biochem 46:265–271Google Scholar
  136. Liu J, Zhang Z, Dang H, Lu J, Cui Z (2011b) Isolation and Characterization of a Cold-Active Amylase from Marine Wangia Sp. C52. Afr J Biotechnol Res 5:1156–1162Google Scholar
  137. Liu Z, Li G, Mo Z, Mou H (2013) Molecular cloning, characterization, and heterologous expression of a new κ-carrageenase gene from marine bacterium Zobellia sp. ZM-2. Appl Microbiol Biotechnol 97:10057–10067Google Scholar
  138. Long J, Wu Z, Li X et al (2015a) New method for the immobilization of pullulanase onto hybrid magnetic (Fe3O4–κ-carrageenan) nanoparticles by electrostatic coupling with pullulanase/chitosan complex. J Agric Food Chem 8:3534–3542Google Scholar
  139. Long J, Yu X, Xu E et al (2015b) In situ synthesis of new magnetite chitosan/carrageenan nanocomposites by electrostatic interactions for protein delivery applications. Carbohydr Polym 131:98–107Google Scholar
  140. Luaces-Rodríguez A, Díaz-Tomé V, González-Barcia M et al (2017) Cysteamine polysaccharide hydrogels: study of extended ocular delivery and biopermanence time by PET imaging. Int J Pharm 528:714–722Google Scholar
  141. Ma YX, Dong SL, Jiang XL, Li J, Mou HJ (2010) Purification and characterization of κ-carrageenase from marine bacterium mutant strain Pseudoalteromonas sp. AJ5-13 and its degraded products. J Food Biochem 34:661–678Google Scholar
  142. Ma S, Duan G, Chai W, Geng C, Tan Y, Wang L, Sourd F, Michel G, Yu W, Han F (2013) Purification, cloning, characterization and essential amino acid residues analysis of a new ι-carrageenase from Cellulophaga sp. QY3. PLoS ONE 8:e64666Google Scholar
  143. Mahdavinia GR, Marandi GB, Pourjavadi A, Kiani G (2010) Semi-IPN carrageenan-based nanocomposite hydrogels: synthesis and swelling behavior. J Appl Polym Sci 118:2989–2997Google Scholar
  144. Makas YG, Kalkan NA, Aksoy S et al (2010) Immobilization of laccase in κ-carrageenan based semi-interpenetrating polymer networks. J Biotechnol 148:216–220Google Scholar
  145. Manivasagan P, Oh J (2016) Marine polysaccharide-based nanomaterials as a novel source of nanobiotechnological applications. Int J Biol Macromol 82:315–327Google Scholar
  146. Mao S, Guo C, Shi Y (2012a) Recent advances in polymeric micro-spheres for parenteral drug delivery-part 1. Expert Opin Drug Deliv 9:1161–1176Google Scholar
  147. Mao S, Guo C, Shi Y, Li LC (2012b) Recent advances in polymeric micro-spheres for parenteral drug delivery-Part 2. Expert Opin Drug Deliv 9:1209–1223Google Scholar
  148. Martin M, Barbeyron T, Michel G, Portetelle D, Vandenbol M (2013) Functional screening of a metagenomic library from algal biofilms. Commun Agric Appl Biol Sci 78:37–41Google Scholar
  149. Martin M, Portetelle D, Michel G, Vandenbol M (2014) Microorganisms living on macroalgae: diversity, interactions, and biotechnological applications. Appl Microbiol Biotechnol 98:2917–2935Google Scholar
  150. Masuda S, Endo K, Koizumi N, Hayami T, Fukazawa T, Yatsunami R, Fukui T, Nakamura S (2006) Molecular identification of a novel beta-1,3-glucanase from alkaliphilic Nocardiopsis sp. strain F96. Extremophiles 10:251–255Google Scholar
  151. Mavromatis K, Abt B, Brambilla E, Lapidus A, Copeland A (2010) Complete genome sequence of Coraliomargarita akajimensis type strain (04OKA010–24). Stand Genom Sci 2:290–299Google Scholar
  152. McDonald HC, Schmidt B (2009) Kappa-carrageenase and kappa-carrageenase containing compositions. US20090048136A1Google Scholar
  153. McGill HC, McMahan CA, Wigodsky HS, Sprinz H (1977) Carrageenan in formula and infant baboon development. Gastroenterology 73:512–517Google Scholar
  154. McKim JM, Baas H, Rice GP et al (2016) Effects of carrageenan on cell permeability, cytotoxicity, and cytokine gene expression in human intestinal and hepatic cell lines. Food Chem Toxicol 96:1–10Google Scholar
  155. McLean MW, Williamson FB (1979) κ-Carrageenase from Pseudomonas carrageenovora. Eur J Biochem 93:553–558Google Scholar
  156. McLean MW, Williamson FB (1981) Enzymes from Pseudomonas carrageenovora. Application to studies of carrageenan structure. Proc Int Seaweed Symp 10:479–484Google Scholar
  157. Mensour NA, Margaritis A, Briens CL, Pilkington H, Russel I (1996) Application of immobilized yeast cells in the brewing industry. Prog Biotechnol 11:661–671Google Scholar
  158. Michel G, Barbeyron T, Flament D, Vernet T, Kloareg B, Dideberg O (1999) Expression, purification, crystallization and preliminary x-ray analysis of the kappa-carrageenase from Pseudoalteromonas carrageenovora. Acta Crystallogr D 55:918–920Google Scholar
  159. Michel G, Flament D, Barbeyron T, Vernet T, Kloareg B, Dideberg O (2000) Expression, purifi cation, crystallization and preliminary X-ray analysis of the iota-carrageenase from Alteromonas fortis. Acta Crystallogr D 56:766–768Google Scholar
  160. Michel G, Chantalat L, Duee E, Barbeyron T, Henrissat B et al (2001a) The kappa carrageenase of P. carrageenovora features a tunnel-shaped active site: a novel insight in the evolution of Clan-B glycoside hydrolases. Structure 9:513–525Google Scholar
  161. Michel G, Chantalat L, Fanchon E, Henrissat B, Kloareg B, Dideberg O (2001b) The ι- carrageenase of Alteromonas fortis. A b-helix fold-containing enzyme for the degradation of a highly polyanionic polysaccharide. J Biol Chem 276:40202–40209Google Scholar
  162. Michel G, Helbert W, Kahn R et al (2003) The structural bases of the processive degradation of ι-carrageenan, a main cell wall polysaccharide of red algae. J Mol Biol 334:421–433Google Scholar
  163. Michel G, Nyval-Collen P, Barbeyron T, Czjzek M, Helbert W (2006) Bioconversion of red seaweed galactans: a focus on bacterial agarases and carrageenases. Appl Microbiol Biotechnol 71:23–33Google Scholar
  164. Miyazaki S, Ishitani M, Takahashi A, Shimoyama T, Itho K, Attwood D (2011) Carrageenan gels for oral sustained delivery of acetaminophen to dysphagicpatients. Biol Pharm Bull 34:164–166Google Scholar
  165. Mohamadnia Z, Zohuriaan-Mehr MJ, Kabiri K, Jamshidi A, Mobedi H (2008) Ionically cross-linked carrageenan-alginate hydrogel beads. Journal of Biomate-rials Science. J Biomater Sci Polym Ed 19:47–59Google Scholar
  166. Moreno-Villoslada I, Oyarzun F, Miranda V, Hess S, Rivas BL (2005) Bind-ing of chlorpheniramine maleate to pharmacologically important alginic acid, carboxymethylcellulose, kappa-carageenan, and iota-carrageenan as studied bydiafiltration. J Appl Polym Sci 98:598–602Google Scholar
  167. Morris CJ (2003) Carrageenan-induced paw edema in the rat and mouse inflammation protocols. Humana Press, New Jersey, pp 115–122Google Scholar
  168. Mou H, Jiang X, Liv Z, Guan H (2004) Structural analysis of kappa-carrageenan oligosaccharides released by carrageenase from marine Cytophaga MCA-2. J Food Biochem 28:245–260Google Scholar
  169. Muffler K, Sana B, Mukherjee J, Ulber R (2015) Marine enzymes—production & applications BT. In: Kim S-K (ed) Springer handbook of marine biotechnology. Springer, Berlin, pp 413–429Google Scholar
  170. Muller I, Kahnert A, Pape T, Sheldrick GM, Meyer-Klaucke W, Dierks T et al (2004) Crystal structure of the alkylsulfatase AtsK: insights into the catalytic mechanism of the Fe(II) alpha-ketoglutarate-dependent dioxygenase superfamily. Biochemistry 43:3075–3088Google Scholar
  171. Myslabodski DE, Stancioff D, Heckert RA (1996) Effect of acid hydrolysis on the molecular weight of kappa carrageenan by GPC-LS. Carbohydr Polym 31:83–92Google Scholar
  172. Navrátil M, Gemeiner P, Klein J et al (2002) Properties of hydrogel materials used for entrapment of microbial cells in production of fermeted beverages. Artif Cells Blood Substit Biotechnol 30:199–218Google Scholar
  173. Necas J, Bartosikova L (2013) Carrageenan: a review. Vet Med (Praha) 58:187–205Google Scholar
  174. Negi S, Banerjee R (2009) Characterization of amylase and protease produced by Aspergillus awamori in a single bioreactor. Food Res Int 42:433–448Google Scholar
  175. Nerurkar J, Jun HW, Price JC, Park MO (2005) Controlled-release matrix tablets of ibuprofen using cellulose ethers and carrageenans: effect of formulation factors on dissolution rates. Eur J Pharm Biopharm 61:56–68Google Scholar
  176. Ni M (2009) Study on κ-carrageenase of marine bacterium Cellulophaga sp. QY201, QingdaoGoogle Scholar
  177. Nigam JN (2000) Continuous ethanol production from pineapple cannery waste using immobilized yeast cells. J Biotechnol 80:189–193Google Scholar
  178. Nikolaivits E, Dimarogona M, Fokialakis N, Topakas E (2017) Marine-derived biocatalysts: importance, accessing, and application in aromatic pollutant bioremediation. Front Microbiol 8:265Google Scholar
  179. Oh C, Kwon YK, Heo SJ, De Zoysa M, Affan A et al (2011) Complete genome sequence of strain s 85, a novel member of the family Flavobacteriaceae. J Bacteriol 193:6107Google Scholar
  180. Ohta Y, Hatada Y (2006) A novel enzyme, lambda-carrageenase isolated from a deep sea bacterium. J Biochem 140:475–481Google Scholar
  181. Østgaard K, Wangen BF, Knutsen SH, Aasen IM (1993) Large-scale production and purification of κ-carrageenase from Pseudomonas carrageenovora for application in seaweed biotechnology. Enzyme Microb Technol 15:326–333Google Scholar
  182. Osuga J, Mori A, Kato J (1984) Acetic acid production by immobilized Acetobacter aceti cells entrapped in a κ-carrageenan gel. J Ferment Technol 62:139–149Google Scholar
  183. Ozsoy Y, Bergisadi N (2000) Preparation of mefenamic acid sustained releasebeads based on kappa-carrageenan. Boll Chim Farm 139:120–123Google Scholar
  184. Padhi JR, Nayak D, Nanda A et al (2016) Development of highly biocompatible Gelatin & i-Carrageenan based composite hydrogels: in depth physiochemical analysis for biomedical applications. Carbohydr Polym 153:292–301Google Scholar
  185. Pairatwachapun S, Paradee N, Sirivat A (2016) Controlled release of acetylsalicylic acid from polythiophene/carrageenan hydrogel via electrical stimulation. Carbohydr Polym 137:214–221Google Scholar
  186. Pati A, Abt B, Teshima H, Nolan M, Lapidus A et al (2011) Complete genome sequence of Cellulophaga lytica type strain (LIM-21). Stand Genom Sci 4:221–232Google Scholar
  187. Patier P, Potin P, Rochas C, Kloareg B, Yvin J-C, Liénart Y (1995) Free and silica-bound oligo kappa-carrageenan elicit laminarinase activity in Rubus cells and protoplasts. Plant Sci 110:27–35Google Scholar
  188. Patil RT, Speaker TJ (1998) Carrageenan as an anionic polymer for aqueous microencapsulation. Drug Deliv 5:179–182Google Scholar
  189. Pavli M, Vrecer F, Baumgartner S (2010) Matrix tablets based on carrageenanswith dual controlled release of doxazosin mesylate. Int J Pharm 400:15–23Google Scholar
  190. Pavli M, Baumgartner S, Kos P, Kogej K (2011) Doxazosin–carrageenan inter-actions: a novel approach for studying drug–polymer interactions and relationto controlled drug release. Int J Pharm 421:110–119Google Scholar
  191. Pedersen G, Hagen HA, Asferg L, Sorensen E (1995) Removal of printing paste thickner and excess dye after textile printing. US5405414AGoogle Scholar
  192. Percival E (1979) The polysaccharides of green, red and brown seaweeds: their basic structure, biosynthesis and function. Br J Psychol 14:103–117Google Scholar
  193. Picker KM (1999a) Matrix tablets of carrageenans. II. Release behavior and effect of added cations. Drug Dev Ind Pharm 25:339–346Google Scholar
  194. Picker KM (1999b) The use of carrageenan in mixture with microcrystalline cellulose and its functionality for making tablets. Eur J Pharm Biopharm 48:27–36Google Scholar
  195. Piyakulawat P, Praphairaksit N, Chantarasiri N, Muangsin N (2007) Preparation and evaluation of chitosan/carrageenan beads for controlled release of sodium diclofenac. AAPS Pharm Sci Tech 8:E97Google Scholar
  196. Popa EG, Gomes ME, Reis RL (2011) Cell delivery systems using alginate-carrageenan hydrogel beads and fibers for regenerative medicine applications. Biomacromol 12:3952–3961Google Scholar
  197. Potin P, Sanseau A, Le Gall Y, Rochas C, Kloareg B (1991) Purification and characterization of a new κ-carrageenase from a marine Cytophaga-like bacterium. Eur J Biochem 201:241–247Google Scholar
  198. Potin P, Richard C, Barbeyron T, Henrissat B, Gey C, Petillot Y, Forest E, Dideberg O, Rochas C, Kloareg B (1995) Processing and hydrolytic mechanism of the cgkA-encoded κ-carrageenase of Alteromonas carrageenovora. Eur J Biochem 228:971–975Google Scholar
  199. Préchoux A, Helbert W (2014) Preparation and detailed NMR analyses of a series of oligo α-carrageenans. Carbohydr Polym 101:864–870Google Scholar
  200. Préchoux A, Genicot S, Rogniaux H, Helbert W (2013) Controlling carrageenan structure using a novel formylglycine-dependent sulfatase, an endo-4S-iota-carrageenan sulfatase. Mar Biotechnol 15:265–274Google Scholar
  201. Préchoux A, Genicot S, Rogniaux H, Helbert W (2016) Enzyme-assisted preparation of furcellaran-like κ-/β-carrageenan. Mar Biotechnol 18:133–143Google Scholar
  202. Pujol CA, Scolaro LA, Ciancia M, Matulewicz MC, Cerezo AS, Damonte EB (2006) Antiviral activity of a carrageenan from Gigartinatina skottsbergii against intraperitoneal murine herpes simplex virus infection. Planta Med 72:121–125Google Scholar
  203. Puligundla P, Poludasu RM, Rai JK, Obulam VSR (2011) Repeated batch ethanolic fermentation of very high gravity medium by immobilized Saccharomyces cerevisiae. Ann Microbiol 61:863–869Google Scholar
  204. Raman M, Devi V, Doble M (2015) Biocompatible ι-carrageenan-γ-maghemite nanocomposite for biomedical applications—synthesis, characterization and in vitro anticancer efficacy. J Nanobiotechnol 13:18Google Scholar
  205. Rebuffet E, Barbeyron T, Jeudy A, Jam M, Czjzek M, Michel G (2010) Identification of catalytic residues and mechanistic analysis of family GH82 iota-carrageenases. Biochemistry 49:7590–7599Google Scholar
  206. Relleve L, Nagasawa N, Luan LQ, Yagi T, Aranilla C, Abad L et al (2005) Degradation of carrageenan by radiation. Polym Degrad Stab 87:403–410Google Scholar
  207. Rhein-Knudsen N, Ale MT, Meyer AS (2015) Seaweed hydrocolloid production: an update on enzyme assisted extraction and modification technologies. Mar Drugs 13:3340–3359Google Scholar
  208. Rhim J-W, Wang L-F (2014) Preparation and characterization of carrageenan-based nanocomposite films reinforced with clay mineral and silver nanoparticles. Appl Clay Sci 97:174–181Google Scholar
  209. Rinas U, Hoffmann F (2004) Selective leakage of host-cell proteins during highcell-density cultivation of recombinant and non-recombinant Escherichia coli. Biotechnol Prog 20:679–687Google Scholar
  210. Rochas C, Lahaye M, Yaphe W (1986) Sulfate content of carrageenan and agar determined by infrared spectroscopy. Bot Mar 29:335–340Google Scholar
  211. Rodrigues S, da Costa AMR, Grenha A (2012) Chitosan/carrageenan nanoparticles: effect of cross-linking with tripolyphosphate and charge ratios. Carbohydr Polym 89:282–289Google Scholar
  212. Rodrigues S, Cordeiro C, Seijo B, Remuñán-López C, Grenha A (2015) Hybrid nanosystems based on natural polymers as protein carriers for respiratory delivery: stability and toxicological evaluation. Carbohydr Polym 123:369–380Google Scholar
  213. Rosario NL, Ghaly ES (2002) Matrices of water-soluble drug using natural polymer and direct compression method. Drug Dev Ind Pharm 28:975–988Google Scholar
  214. Rouzbehan S, Moein S, Homaei A, Moein MR (2017) Kinetics of α-glucosidase inhibition by different fractions of three species of Labiatae extracts: a new diabetes treatment model. Pharm Biol 55:1483–1488Google Scholar
  215. Running CA, Falshaw R, Janaswamy S (2012) Trivalent iron induced gelation in lambda-carrageenan. Carbohydr Polym 87:2735–2739Google Scholar
  216. Sankalia MG, Mashru RC, Sankalia JM, Sutariya VB (2006a) Physicochemical characterization of papain entrapped in ionotropically cross-linked kappa-carrageenan gel beads for stability improvement using Doehlert shell design. J Pharm Sci 95:1994–2013Google Scholar
  217. Sankalia MG, Mashru RC, Sankalia JM, Sutariya VB (2006b) Stability improvement of alpha-amylase entrapped in kappa-carrageenan beads: physicochemical characterization and optimization using composite index. Int J Pharm 312:1–14Google Scholar
  218. Santo VE, Frias AM, Carida M et al (2009) Carrageenan-based hydrogels for the controlled delivery of PDGF-BB in bone tissue engineering applications. Biomacromol 10:1392–1401Google Scholar
  219. Sarwar G, Matayoshi S, Oda H (1987) Purification of κ-carrageenase from marine Cytophaga species. Microbiol Immunol 31:869–877Google Scholar
  220. Sathuvan M, Thangam R, Gajendiran M et al (2017) κ-carrageenan: an effective drug carrier to deliver curcumin in cancer cells and to induce apoptosis. Carbohydr Polym 160:184–193Google Scholar
  221. Selvakumaran S, Muhamad II, Abd Razak SI (2016) Evaluation of kappa carrageenan as potential carrier for floating drug delivery system: effect of pore forming agents. Carbohydr Polym 135:207–214Google Scholar
  222. Sharifian S, Homaei A, Hemmati R, Khajeh K (2017) Light emission miracle in the sea and preeminent applications of bioluminescence in recent new biotechnology. J Photochem Photobiol B Biol 172:115–128Google Scholar
  223. Sharifzadeh G, Wahit MU, Soheilmoghaddam M et al (2016) Kappa-carrageenan/halloysite nanocomposite hydrogels as potential drug delivery systems. J Taiwan Inst Chem Eng 67:426–434Google Scholar
  224. Shojaei F, Homaei A, Taherizadeh MR, Kamrani E (2017) Characterization of Biosynthesized chitosan nanoparticles from Penaeus vannamei for immobilization of P. vannamei protease: an eco-friendly nanobiocatalyst. Int J Food Prop.  https://doi.org/10.1080/10942912.2017.1345935 CrossRefGoogle Scholar
  225. Sjöberg H, Persson S, Caram-Lelham N (1999) How interactions between drugs and agarose-carrageenan hydrogels influence the simultaneous transport of drugs. J Control Release 59:391–400Google Scholar
  226. Smith RG, Bidwell RGS (1989) Inorganic carbon uptake by photosynthetically active protoplasts of the red macroalga Chondrus crispus. Mar Biol 102:1–4Google Scholar
  227. Snelgrove P (2016) An ocean of discovery: biodiversity beyond the census of marine life. Planta Med 82:790–799Google Scholar
  228. Sodini I, Boquien CY, Corrieu G, Lacroix C (1997a) Use of an immobilized cell bioreactor for the continuous inoculation of milk in fresh cheese manufacturing. J Ind Microbiol Biotechnol 18:56–61Google Scholar
  229. Sodini I, Boquien CY, Corrieu G, Lacroix C (1997b) Microbial dynamics of co- and separately entrapped mixed cultures of mesophilic lactic acid bacteria during the continuous prefermentation of milk. Enzyme Microb Technol 20:381–388Google Scholar
  230. Sroka P, Satora P, Tarko T, Duda-Chodak A (2017) The influence of yeast immobilization on selected parameters of young meads. J Inst Brew 123:289–295Google Scholar
  231. Sun F, Ma Y, Wang Y, Liu Q (2010) Purification and characterization of novel κ-carrageenase from marine Tamlana sp. HC4. Chin J Oceanol Limnol 28:1139–1145Google Scholar
  232. Sun Y, Liu Y, Jiang K et al (2014) Electrospray Ionization mass spectrometric analysis of κ-carrageenan oligosaccharides obtained by degradation with κ-carrageenase from Pedobacter hainanensis. J Agric Food Chem 62:2398–2405Google Scholar
  233. Sun Y, Yang B, Wu Y, Liu Y, Gu X, Zhang H, Wang C, Cao H, Huang L, Wang Z (2015) Structural characterization and antioxidant activities of κ-carrageenan oligosaccharides degraded by different methods. Food Chem 178:311–318Google Scholar
  234. Swain MR, Natarajan V, Krishnan C (2017) Bioethanol from marine sources marine enzymes and microorganisms for bioethanol production. In: Advances in food and nutrition research, pp 181–197Google Scholar
  235. Talarico LB, Damonte EB (2007) Interference in dengue virus adsorption and uncoating by carrageenans. Virology 363:473–485Google Scholar
  236. Talarico LB, Noseda MD, Ducatti DRB, Duarte ME, Damonte EB (2011) Differential inhibition of dengue virus infection in mammalian and mosquito cells by iota-carrageenan. J Gen Virol 92:1332–1342Google Scholar
  237. Tang J, Wang M, Zhou Q, Nagata S (2011) Improved composting of Undaria pinnatifida seaweed by inoculation with Halomonas and Gracilibacilus sp. isolated from marine environments. Bioresour Technol 102:2925–2930Google Scholar
  238. Tapia C, Escobar Z, Costa E, Sapag-Hagar J, Valenzuela F, Basualto C, Gai MN, Yazdani-Pedram M (2004) Comparative studies on polyelectrolyte complexes and mixtures of chitosan-alginate and chitosan-carrageenan as prolonged diltiazem clorhydrate release systems. Eur J Pharm Biopharm 57:65–75Google Scholar
  239. Tapia C, Corbalán V, Costa E et al (2005) Study of the release mechanism of diltiazem hydrochloride from matrices based on chitosan alginate and chitosan carrageenan mixtures. Biomacromol 6:2389–2395Google Scholar
  240. Thakur NL, Thakur A (2006) Marine biotechnology: an overview. Indian J Biotechnol 5:263–268Google Scholar
  241. Therkelsen GH (1993) Cangeenan. In: Whistler RL, BeMiller JN (eds) Industrial gums polysaccharide derivatives. Academic Press, San Diego, pp 145–180Google Scholar
  242. Thrash JC, Cho JC, Vergin KL, Morris RM, Giovannoni SJ (2010) Genome sequence of Lentisphaera araneosa HTCC2155T, the type species of the order Lentisphaerales in the phylum Lentisphaerae. J Bacteriol 192:2938–2939Google Scholar
  243. Thrimawithana TR, Young SA, Bunt CR, Green CR, Alany RG (2011) In-vitro and in vivo evaluation of carrageenan/methylcellulose polymeric systemsfor transscleral delivery of macromolecules. Eur J Pharm Sci 44:399–409Google Scholar
  244. Tobacman JK (2001) Review of harmful gastrointestinal effects of carrageenan in animal experiments. Environ Health Perspect 109:983–994Google Scholar
  245. Tomoda K, Asahiyama M, Ohtsuki E et al (2009) Preparation and properties of carrageenan microspheres containing allopurinol and local anesthetic agents for the treatment of oral mucositis. Colloids Surf B Biointerfaces 71:27–35Google Scholar
  246. Trincone A (2013) Biocatalytic processes using marine biocatalysts: ten cases in point. Curr Org Chem 17:1058–1066Google Scholar
  247. Trincone A (2017) Enzymatic processes in marine biotechnology. Mar Drugs 15:93Google Scholar
  248. Tuleu C, Khela MK, Evans DF, Jones BE, Nagata S, Basit AW (2007) Ascintigraphic investigation of the disintegration behaviour of capsules in fastingsubjects: a comparison of hypromellose capsules containing carrageenan as agelling agent and standard gelatin capsules. Eur J Pharm Sci 30:251–255Google Scholar
  249. Vadlapatla R, Fifer EK, C-j Kim, Alexander KS (2009) Drug-organic electrolyte complexes as controlled release systems. Drug Dev Ind Pharm 35:1–11Google Scholar
  250. Van De Velde F, Peppelman HA, Rollema HS, Hans R (2001) On the structure of κ/ι-hybrid carrageenans. Carbohydr Res 331:271–283Google Scholar
  251. Van de Velde F, Knutsen SH, Usov AI, Rollema HS, Cerezo AS (2002a) 1H and 13C high resolution NMR spectroscopy of carrageenans: application in research and industry. Trends Food Sci Technol 13:73–92Google Scholar
  252. van de Velde F, Lourenço ND, Pinheiro HM (2002b) Carrageenan: a food-grade and biocompatible support for immobilisation techniques. Adv Synth Catal 334:815–835Google Scholar
  253. Vauthier C, Bouchemal K (2009) Methods for the preparation and manufacture of polymeric nanoparticles. Pharm Res 26:1025–1058Google Scholar
  254. Venkatesan J, Anil S, Kim S-K, Shim M (2016) Seaweed polysaccharide-based nanoparticles: preparation and applications for drug delivery. Polymers (Basel) 8:30Google Scholar
  255. Venugopal V (2011) Polysaccharide from seaweed and microalgae. In: Zollo S (ed) Marine polysaccharides. Taylor and Francis Group, Boca Raton, pp 111–122Google Scholar
  256. Wang Y-Z, Liao Q, Zhu X et al (2010) Characteristics of hydrogen production and substrate consumption of Rhodopseudomonas palustris CQK 01 in an immobilized-cell photobioreactor. Bioresour Technol 101:4034–4041Google Scholar
  257. Wang W, Zhang P, Hao C, Zhang X-E, Cui Z-Q, Guan H-S (2011) In vitro inhibitory effect of carrageenan oligosaccharide on influenza A H1N1 virus. Antiviral Res 92:237–246Google Scholar
  258. Wang W, Zhang P, Yu G-L, Li C-X, Hao C, Qi X, Zhang L-J, Guan H-S (2012) Preparation and anti-influenza A virus activity of κ-carrageenan oligosaccharide and its sulphated derivatives. Food Chem 133:880–888Google Scholar
  259. Wang T, Hu Q, Zhou M et al (2016) Preparation of ultra-fine powders from polysaccharide-coated solid lipid nanoparticles and nanostructured lipid carriers by innovative nano spray drying technology. Int J Pharm 511:219–222Google Scholar
  260. Wecker P, Klockow C, Schüler M, Dabin J, Michel G, Glöckner FO (2010) Life cycle analysis of the model organism Rhodopirellula baltica SH 1T by transcriptome studies. Microb Biotechnol 3:583–594Google Scholar
  261. Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9:2707–2719Google Scholar
  262. Weigl J, Yaphe W (1966) The enzymatic hydrolysis of carrageenan by Pseudomonas carrageenovora: purification of a κ-carrageenase. Can J Microbiol 12:939–947Google Scholar
  263. Weiner ML (2014) Food additive carrageenan: part II: A critical review of carrageenan in vivo safety studies. Crit Rev Toxicol 44:244–269Google Scholar
  264. Weiner ML (2016) Parameters and pitfalls to consider in the conduct of food additive research, Carrageenan as a case study. Food Chem Toxicol 87:31–44Google Scholar
  265. Weiner ML, Ferguson HE, Thorsrud BA et al (2015) An infant formula toxicity and toxicokinetic feeding study on carrageenan in preweaning piglets with special attention to the immune system and gastrointestinal tract. Food Chem Toxicol 77:120–131Google Scholar
  266. Wijesekara I, Pangestuti R, Kim S-K (2011) Biological activities and potentialhealth benefits of sulfated polysaccharides derived from marine algae. Carbohydr Polym 84:14–21Google Scholar
  267. Wu S-J (2012) Degradation of κ-carrageenan by hydrolysis with commercial á-amylase. Carbohydr Polym 89:394–396Google Scholar
  268. Xu C, Zhu Y, Ni H, Cai H, Li L, Xiao A (2015) Isolation, identification of a κ-carrageenase-producing bacterium and κ-carrageenase characterization. Wei Sheng Wu Xue Bao = Acta Microbiol Sinica 55:140–148Google Scholar
  269. Yamada T, Ogamo A, Saito T, Watanabe J, Uchiyama H, Nakagawa Y (1997) Preparation and anti-HIV activity of low-molecular-weight carrageenans and their sulfated derivatives. Carbohydr Polym 32:51–55Google Scholar
  270. Yamada T, Ogamo A, Saito T, Uchiyama H, Nakagawa Y (2000) Preparation of O-acylated low-molecular-weight carrageenans with potent anti-HIV activity and low anticoagulant effect. Carbohydr Polym 41:115–120Google Scholar
  271. Yao Z, Zhang C, Lu F, Bie X, Lu Z (2012) Gene cloning, expression, and characterization of a novel acetaldehyde dehydrogenase from Issatchenkia terricola strain XJ-2. Appl Microbiol Biotechnol 5:1999–2009Google Scholar
  272. Yao Z, Wang F, Gao Z, Jin L, Wu H (2013) Characterization of a κ-carrageenase from marine Cellulophaga lytica strain N5-2 and analysis of its degradation products. Int J Mol Sci 14:24592–24602Google Scholar
  273. Yao Z, Wu H, Zhang S, Du Y (2014) Enzymatic preparation of κ-carrageenan oligosaccharides and their anti-angiogenic activity. Carbohydr Polym 30:359–367Google Scholar
  274. Yilmaz P, Kottmanna R, Pruesse E, Quast C, Oliver Glöckne F (2011) Analysis of 23S rRNA genes in metagenomes—a case study from the Global Ocean Sampling Expedition. Syst Appl Microbiol 34:462–469Google Scholar
  275. Youssef AS, Beltagy EA, El-Shenawy MA (2012) Production of κ-carrageenase by Cellulosimicrobium cellulans isolated from Egyptian Mediterranean coast. Afr J Microbiol Res 6:6618–6628Google Scholar
  276. Yuan Y, Luan X, Rana X et al (2017) Covalent immobilization of cellulase in application of biotransformation of ginsenoside Rb1. J Mol Catal B Enzym 133:S525–S532Google Scholar
  277. Yun EJ, Kim HT, Cho KM et al (2016) Pretreatment and saccharification of red macroalgae to produce fermentable sugars. Bioresour Technol 199:311–318Google Scholar
  278. Zablackis E, Vreeland V, Kloareg B (1993) Isolation of protoplasts from kappaphycus alvarezii var. tambalang (Rhodophyta) and secretion of carrageenan fragments by cultured cells. J Exp Bot 44:1515–1522Google Scholar
  279. Zeinali F, Homaei A, Kamrani E (2015) Sources of marine superoxide dismutases: characteristics and applications. Int J Biol Macromol 79:627–637Google Scholar
  280. Zhang C, Kim SK (2010) Research and application of marine microbial enzymes: status and prospects. Mar Drugs 8:1920–1934Google Scholar
  281. Zhang Z, Zhang R, Chen L, McClements DJ (2016) Encapsulation of lactase (β-galactosidase) into κ-carrageenan-based hydrogel beads: impact of environmental conditions on enzyme activity. Food Chem 200:69–75Google Scholar
  282. Zhou MH, Ma JS, Li J, Ye H, Huang K, Zhao X (2008) A kappa-carrageenase from a newly isolated Pseudoalteromonas-like bacterium, WZUC10. Biotechnol Bioprocess Eng 13:545–551Google Scholar
  283. Zhu B, Ning L (2016) Purification and characterization of a New κ-carrageenase from the marine bacterium Vibrio sp. NJ-2. J Microbiol Biotechnol 26:255–262Google Scholar
  284. Zia KM, Tabasum S, Nasif M et al (2017) A review on synthesis, properties and applications of natural polymer based carrageenan blends and composites. Int J Biol Macromol 96:282–301Google Scholar
  285. Ziayoddin M, Lalitha J, Shinde M (2014) Increased production of carrageenase by Pseudomonas aeruginosa ZSL-2 using Taguchi experimental design. Int Lett Nat Sci 12:194–207Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Marine Biology, Faculty of SciencesUniversity of HormozganBandar AbbasIran
  2. 2.Department of Fisheries, Faculty of SciencesUniversity of HormozganBandar AbbasIran
  3. 3.Department of Biochemistry, Faculty of SciencesUniversity of HormozganBandar AbbasIran

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