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Carrageenanolytic enzymes from marine bacteria associated with the red alga Tichocarpus crinitus

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Abstract

One hundred six bacterial strains (106 strains) were isolated from the Pacific red alga Tichocarpus crinitus, collected from the Troitsa Bay of Gulf of Peter the Great (Sea of Japan, Russia), and studied on their ability to degrade different samples of carrageenan as substrates. Some of the studied strains exhibited hydrolytic activity selectively to a total polysaccharide (kappa and lambda) from Chondrus armatus, other strains, to κ/β-carrageenan from T. crinitus, which did not possess the same effect to a total polysaccharide from T. crinitus. The strains with the highest enzyme activity (28 strains) were identified using 16S rRNA gene sequence techniques and classified to the phyla Bacteroidetes and Proteobacteria. Most (75%) of the studied carrageenase producers belong to phylum Bacteroidetes (21 strains). These strains were related with 7 phylotypes of the genera Aquimarina, Cellulophaga, Maribacter, and Zobellia (family Flavobacteriaceae of the class Flavobacteriia). Cellulophaga strains were the dominant group (35.7% of total) and closely related to species C. baltica and C. lytica with 99.8 and 99.9% sequence similarity, respectively. The remaining strains (7 strains) were represented by members of the genera Altererythrobacter (the family Erythrobacteraceae), Phaeobacter, Sulfitobacter, Tateyamaria (the family Rhodobacteraceae), and Sphingomonas (the family Sphingobacteriaceae) of the class Alphaproteobacteria and Psychrobacter (the family Moraxellaceae) and Vibrio (the family Vibrionaceae) of the class Gammaproteobacteria.

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References

  • Anastyuk SD, Barabanova AO, Correc G, Nazarenko EL, Davydova VN, Helbertb W, Dmitrenok PS, Yermak IM (2011) Analysis of structural heterogeneity of κ/β-carrageenan oligosaccharides from Tichocarpus crinitus by negative-ion ESI and tandem MALDI mass spectrometry. Carbohydr Polym 86:546–554

    Article  CAS  Google Scholar 

  • Barabanova AO, Yermak IM, Glazunov VP, Isakov VV, Titlyanov EA, Solov’eva TF (2005) Comparative study of carrageenans from reproductive and sterile forms of Tichocarpus crinitus (Gmel.) Rupr (Rhodophyta, Tichocarpaceae). Biochemist 70:350–356

    CAS  Google Scholar 

  • Barabanova AO, Shashkov AS, Glazunov VP, Isakov VV, Nebylovskaya TB, Helbert W, Solov’eva TF, Yermak IM (2008) Structure and properties of carrageenan-like polysaccharide from the red alga Tichocarpus crinitus (Gmel.) Rupr. (Rhodophyta, Tichocarpaceae). J Appl Phycol 20:1013–1020

    Article  CAS  Google Scholar 

  • Barbeyron T, Gerard A, Potin P, Henrissat B, Kloareg B (1998) The kappa- carrageenase of the marine bacterium Cytophaga drobachiensis. Structural and phylogenetic relationships within family-16 glycoside hydrolases. Mol Biol Evol 15:528–537

    Article  PubMed  CAS  Google Scholar 

  • Bellion C, Brigand G, Prome JC, Bociek DW (1983) Identification et caractérisation des précurseurs biologiques descarraghénanes par spectroscopie de RMN–13. Carbohydr Res 119:31–48

    Article  CAS  Google Scholar 

  • Bhattacharyya S, Liu H, Zhang Z, Jam M, Dudeja PK, Michel G, Linhardt RJ, Tobacman JK (2010) Carrageenan-induced innate immune response is modified by enzymes that hydrolyze distinct galactosidic bonds. J Nutr Biochem 10:906–913

    Article  CAS  Google Scholar 

  • Boulho R, Marty C, Freile-Pelegrín Y, Robledo D, Bourgougnon N, Bedoux G (2017) Antiherpetic (HSV-1) activity of carrageenans from the red seaweed Solieria chordalis (Rhodophyta, Gigartinales) extracted by microwave-assisted extraction (MAE). J Appl Phycol 29:2219–2228

    Article  CAS  Google Scholar 

  • Chauhan PS, Saxena A (2016) Bacterial carrageenases: an overview of production and biotechnological applications. Biotech 6:146

    Google Scholar 

  • Collén PN, Lemoine M, Daniellou R, Guégan JP, Paoletti S, Helbert W (2009) Enzymatic degradation of κ-сarrageenan in aqueous solution. Biomacromolecules 10:1757–1767

    Article  PubMed  CAS  Google Scholar 

  • Coutinho PM, Henrissat B (1999) Carbohydrate-active enzymes: an integrated database approach. In: Gilbert HJ, Davies G, Henrissat B, Svensson B (eds) Recent advances in carbohydrate bioengineering. The Royal Society of Chemistry, Cambridge, pp 3–12

    Google Scholar 

  • Craigie JS (1990) Cell walls. In: Cole KM, Sheath G (eds) Biology of the Red Algae. Cambridge University Press, Cambridge, pp 221–257

    Google Scholar 

  • Feixue S, Yuexin MA, Ying W, Qian L (2010) Purification and characterization of novel k-carrageenase from marine Tamlana sp. HC4. Chin J Ocean Limnol 28:1139–1145

    Article  CAS  Google Scholar 

  • Ghosh T, Chattopadhyay K, Marschall M, Karmakar P, Mandal P, Ray B (2009) Focus on antivirally active sulfated polysaccharides: from structure-activity analysis to clinical evaluation. Glycobiology 19:2–15

    Article  PubMed  CAS  Google Scholar 

  • Groisillier A, Labourel A, Michel G, Tonon T (2015) The mannitol utilization system of the marine bacterium Zobellia galactanivorans. Appl Environ Microbiol 81:1799–1812

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guibet M, Colin S, Barbeyron T, Genicot S, Kloareg B, Michel G, Helbert W (2007) Degradation of λ-carrageenan by Pseudoalteromonas carrageenovora λ-carrageenase: a new family of glycoside hydrolases unrelated to κ- and ι-carrageenases. J Biochem 404:105–114

    Article  CAS  Google Scholar 

  • Hatada Y, Mizuno M, Li Z, Ohta Y (2011) Hyper-production and characterization of the i-carrageenase useful for i-carrageenan oligosaccharide production from a deep-sea bacterium, Microbulbifer thermotolerans JAMB-A94T, and insight into the unusual catalytic mechanism. Mar Biotechnol 13:411–422

    Article  PubMed  CAS  Google Scholar 

  • Kang S, Kim JK (2015) Reuse of seaweed waste by a novel bacterium, Bacillus sp. SYR4 isolated from a sandbar. World J Microbiol Biotechnol 31:209–217

    Article  PubMed  Google Scholar 

  • Khambhaty Y, Mody K, Jha B (2007) Purification and characterization of κ -carrageenase from a novel γ -proteobacterium, Pseudomonas elongata (MTCC 5261) syn. Microbulbifer elongatus comb. nov. Biotechnol Bioprocess Eng 12:668–675

    Article  CAS  Google Scholar 

  • Kim JH, Byun DS, Godber JS, Choi JS, Choi WC, Kim HR (2004) Purification and characterization of arylsulfatase from Sphingomonas sp. AS6330. Appl Microbiol Biotechnol 63:553–559

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  PubMed  CAS  Google Scholar 

  • Knutsen SH, Myslabodski DE, Larsen B, Usov AI (1994) A modified system of nomenclature for red algal galactans. Bot Mar 37:163–169

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  PubMed  CAS  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175

    Google Scholar 

  • Lemoine M, Collen PN, Helbert W (2009) Physical state of κ-carrageenan modulates the mode of action of κ-carrageenase from Pseudoalteromonas carrageenovora. J Biochem 419:545–553

    Article  CAS  Google Scholar 

  • Li J, Hu Q, Seswita-Zilda D (2014) Purification and characterization of a thermostable κ-carrageenase from a hot spring bacterium, Bacillus sp. Biotechnol Lett 36:1669–1674

    Article  PubMed  CAS  Google Scholar 

  • 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 50:799–806

    Article  CAS  Google Scholar 

  • Liu Z, Guiyang 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 97:10057–10067

    Article  PubMed  CAS  Google Scholar 

  • Liu G, Wu S, Jin W, Sun C (2016) Amy63, a novel type of marine bacterial multifunctional enzyme possessing amylase, agarase and carrageenase activities. Sci Rep 6:18726

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martin M, Barbeyron T, Martin R, Portetelle D, Michel G, Vandenbol M (2015) The cultivable surface microbiota of the brown alga Ascophyllum nodosum is enriched in macroalgal-polysaccharide-degrading bacteria. Front Microbiol 6:1487

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin M, Vandermies M, Joyeux C, Martin R, Barbeyron T, Michel G, Vandenbol M (2016) Discovering novel enzymes by functional screening of plurigenomic libraries from alga-associated Flavobacteriia and Gammaproteobacteria. Microbiol Res 186–187:52–61

    Article  PubMed  CAS  Google Scholar 

  • Michel G, Chantalat L, Fanchon E, Henrissat B, Kloareg B, Dideberg O (2001a) The carrageenase of Alteromonas fortis a β-helix fold-containing enzyme for the degradation of a highly polyanionic polysaccharides. J Biol Chem 276:40202–40209

    Article  PubMed  CAS  Google Scholar 

  • Michel G, Chantalat L, Fanchon E, Henrissat B, Kloareg B, Dideberg O (2001b) The ι-carrageenase of Alteromonas fortis. J Biol Chem 276:40202–40209

    Article  PubMed  CAS  Google Scholar 

  • 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 12:23–33

    Article  CAS  Google Scholar 

  • Mou H, Jiang X, Guan H (2003) A-carrageenan derived oligosaccharide prepared by enzymatic degradation containing anti-tumor activity. J Appl Phycol 15:297–303

    Article  CAS  Google Scholar 

  • Mou H, Jiang X, Liu Z, Guan H (2004) Structural analysis of kappa-carrageenan oligosaccharides released by carrageenase from marine Cytophaga MCA-2. J Food Biochem 28:245–260

    Article  CAS  Google Scholar 

  • Ohta Y, Hatada Y (2006) A novel enzyme κ-carrageenase isolated from a deep-sea bacterium. J Biochem 140:475–481

    Article  PubMed  CAS  Google Scholar 

  • Ostgaard KB, Wangen F, Knutsen SH, Aasen IM (1993) Large-scale production and purification of κ-carrageenase from Pseudomonas carrageenorora for applications in seaweed biotechnology. Enzym Microb Technol 15:326–333

    Article  Google Scholar 

  • Park JT, Johnson MJ (1949) A submicro determination of glucose. J Biol Chem 181(1):149–151

    PubMed  CAS  Google Scholar 

  • 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 201:241–247

    Article  PubMed  CAS  Google Scholar 

  • Rebuffet E, Barbeyron T, Jeudy A, Jam M, Czjzek M, Michel G (2010) Identification of catalytic residues and mechanistic analysis of family GH82 ι-carrageenases. Biochemist 49:7590–7599

    Article  CAS  Google Scholar 

  • Rees DA (1963) The carrageenans system of polysaccharides. 1. The relation between the K- and A-components. J Chem Soc 1:1821–1832

    Article  Google Scholar 

  • Renn DW, Santos GA, Dumont LE, Parent CA, Stanley NF, Stancioff DJ, Guiseley KB (1993) β-carrageenan: isolation and characterization. Carbohydr Polym 22:247–252

  • Rochas C, Rinaudo M, Landry S (1990) Role of the molecular-weight on the mechanical-properties of kappa-carrageenan gels. Carbohydr Polym 12:255–266

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Sarwar G, Sakata T, Kakimoto D (1983) The production and characteristics of carrageenase from marine Cytophaga. Bull Jpn Soc Sci Fish 49:1689–1694

    Article  CAS  Google Scholar 

  • Sarwar G, Matayoshi S, Oda H (1987) Purification of a κ-carrageenase from marine Cytophaga species. Microbiol Immunol 31:869–877

    Article  PubMed  CAS  Google Scholar 

  • Shangyong LI, Panpan JIA, Linna W, Wengong YU, Feng H (2013) Purification and characterization of a new thermostable κ-carrageenase from the marine bacterium Pseudoalteromonas sp. QY203. J Ocean Univ China 12:155–159

    Article  CAS  Google Scholar 

  • Soares F, Fernandes C, Silva P, Pereira L, Gonçalves T (2016) Antifungal activity of carrageenan extracts from the red alga Chondracanthus teedei var. lusitanicus. J Appl Phycol 28:2991–2998

    Article  Google Scholar 

  • Sun Y, Liu Y, Jiang K, Wang C, Wang Z, Huang L (2014) Electrospray ionization mass spectrometric analysis of κ-carrageenan oligosaccharides obtained by degradation with κ- carrageenase from Pedobacter hainanensis. J Agric Food Chem 62:2398–2405

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526

    PubMed  CAS  Google Scholar 

  • Tayco CC, Tablizo FA, Regalia RS, Lluisma AO (2013) Characterization of a κ-carrageenase-producing marine bacterium, isolate ALAB-001. Philipp J Sci 142:45–54

    Google Scholar 

  • Usov AI (2011) Polysaccharides of the red algae. Adv Carbohydr Chem Biochem 65:115–217

    Article  PubMed  CAS  Google Scholar 

  • Van de Velde F, Peppelman HA, Rollema HS, Tromp RH (2001) On the structure of κ/ι-hybrid carrageenans. Carbohydr Res 331:271–283

    Article  PubMed  Google Scholar 

  • Wang L, Li S, Zhang S, Li J, Yu W, Gong Q (2015) A new κ-carrageenase CgkS from marine bacterium Shewanella sp. Kz7. J Ocean Univ China 14:759–763

    Article  CAS  Google Scholar 

  • Xu X, Li S, Yang X, Yu W, Han F (2015) Cloning and characterization of a new κ-carrageenase gene from marine bacterium Pseudoalteromonas sp. QY203. J Ocean Univ China 14:1082–1086

    Article  CAS  Google Scholar 

  • Yermak IM, Kim YH, Titlynov EA, Isakov VV, Solov’eva TF (1999) Chemical structure and gel properties of carrageenans from algae belonging to the Gigartinaceae and Tichocarpaceae collected from the Russian Pacific coast. J Appl Phycol 11:41–48

    Article  CAS  Google Scholar 

  • Yermak IM, Barabanova AO, Aminin DL, Davydova VN, Sokolova EV, Solov’eva TF, Kim YH, Shin KS (2012) Effects of structural peculiarities of carrageenans on their immunomodulatory and anticoagulant activities. Carbohydr Polym 87:713–720

    Article  CAS  Google Scholar 

  • Yermak IM, Sokolova EV, Davydova VN, Solov’eva TF, Aminin DL, Reunov AV, Lapshina LA (2016) Influence of red algal polysaccharides on biological activities and supramolecular structure of bacterial lipopolysaccharide. J Appl Phycol 28(1):619–627

  • Youssef AS, Beltagy EA, El-Shenawy MA, El-Assar SA (2012) Production of k-carrageenase by Cellulosimicrobium cellulans isolated from Egyptian Mediterranean coast. Afr J Microbiol Res 6:6618–6628

    Article  CAS  Google Scholar 

  • Yu G, Guan H, Ioanoviciu AS, Sikkander SA, Thanawiroon C, Tobacman JK, Toida T, Linhardt RJ (2002) Structural studies on κ-carrageenan derived oligosaccharides. Carbohydr Res 337:433–440

    Article  PubMed  CAS  Google Scholar 

  • Yuan H, Song J, Li X, Li N, Liu S (2011) Enhanced immunostimulatory and antitumor activity of different derivatives of κ-carrageenan oligosaccharides from Kappaphycus striatum. J Appl Phycol 23:59–65

    Article  CAS  Google Scholar 

  • Zhu B, Ning L (2016) Purification and characterization of a new κ-carrageenase from the marine bacterium Vibrio sp. NJ-2. J Microbiol Biotechnol 26:255–262

    Article  PubMed  CAS  Google Scholar 

  • Ziayoddin M, Shinde M, Lalitha J (2012) Orthogonal array approach for optimization of carrageenase production by solid state fermentation of Pseudomonas aeruginosa ZSL-2. J Microb Biochem Technol 4:4

    Google Scholar 

  • Zuniga EA, Matsuhiro B, Mejias E (2006) Preparation of low-molecular weight fraction by free radical depolymerization of the sulfated galactan from Schizymenia binderi (Gigartinales, Rhodophyta) and its anticoagulant activity. Carbohydr Polym 144:208–215

    Article  CAS  Google Scholar 

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Funding

This work was supported by the Russian Scientific Fund project 14-50-00034. This work (the part related with isolation and characterisation of carrageenan samples) was supported by the Russian Scientific Fund project 16-14-00051.

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Authors and Affiliations

  1. School of Biomedicine, School of Natural Sciences, Far Eastern Federal University, 8 Sukhanova Street, Vladivostok, 690950, Russia

    A. A. Kalitnik & A. D. Kukhlevskiy

  2. G.B. Elyakov Pacific Institute of Bioorganic Chemistry, FEB RAS, 100-let Vladivostoku Prospect, Vladivostok, 690022, Russia

    O. I. Nedashkovskaya, A. M. Stenkova & I. M. Yermak

  3. A.V. Zhirmunsky Institute of Marine Biology, FEB RAS, Pal’chevskogo St. 17, Vladivostok, 690032, Russia

    A. D. Kukhlevskiy

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  1. A. A. Kalitnik
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  2. O. I. Nedashkovskaya
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  4. I. M. Yermak
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Kalitnik, A.A., Nedashkovskaya, O.I., Stenkova, A.M. et al. Carrageenanolytic enzymes from marine bacteria associated with the red alga Tichocarpus crinitus . J Appl Phycol 30, 2071–2081 (2018). https://doi.org/10.1007/s10811-017-1355-4

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  • DOI: https://doi.org/10.1007/s10811-017-1355-4

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