Abstract
Biomass feedstock is an efficient and harmless source of energy. There are various sources of feedstock, such as plant, microbial, macro, and microalgae, and agricultural waste. The major component in biomass feedstock material is a polysaccharide, such as cellulose, cellobiose, starch, and alginate. Alginate is mainly found in macroalgae as one of the significant polysaccharide components. It is made up of β-d-mannuronate (M) and α-l-guluronate (G) blocks. Alginate lyase is an enzyme that degrades alginate by breaking the glycosidic linkage between the poly M and G blocks to liberate oligosaccharides. Several organisms, including bacteria, fungi, viruses, and algae can produce alginate lyases. The species of bacteria, such as Bacillus, Vibrio, Pseudomonas, and Microbulbifer, are some of the important sources of alginate lyases. They are industrially essential enzymes used in food, biofuel, and biomedical industries. There are various assays available to determine the alginate lyase activity qualitatively as well as quantitatively. Qualitatively, different dyes like Gram’s iodine, cetyl pyridinium chloride, and rutanium red can be used to visualize the zone formed due to the alginate lyase activity. DNS assay, UV absorption, and the Somogyi-Nelson method help to determine the alginate lyase activity quantitatively. Since the alginate lyase production in the native organisms is relatively lower, the genes encoding alginate lyases are heterologously cloned and expressed in E. coli to maximize the production and to characterize the enzyme. Different chromatographic techniques like size exclusion, affinity, gel permeation, and ion-exchange chromatography are used to purify the protein. In this paper, the source of alginate and alginate lyases, the mechanism of action of the enzyme, the engineering approaches to enhance the enzyme production, its purification strategy, and the potential applications of alginate lyases has been discussed.
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22 July 2020
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References
Antonopoulou G, Gavala HN, Skiadas IV et al (2008) Biofuels generation from sweet sorghum: fermentative hydrogen production and anaerobic digestion of the remaining biomass. Bioresour Technol 99:110–119. https://doi.org/10.1016/j.biortech.2006.11.048
Bai S, Chen H, Zhu L, Liu W, Yu HD, Wang X, Yin Y (2017) Comparative study on the in vitro effects of Pseudomonas aeruginosa and seaweed alginates on human gut microbiota. PLoS One 12:1–15. https://doi.org/10.1371/journal.pone.0171576
Baron AJ, Wong TY, Hicks SJ et al (1994) Alginate lyase from Klebsiella pneumoniae, subsp. aerogenes: gene cloning, sequence analysis and high-level production in Escherichia coli. Gene 143:61–66. https://doi.org/10.1016/0378-1119(94)90605-X
Beltagy EA, El-Borai A, Lewiz M, ElAssar SA (2016) Purification and characterization of alginate lyase from locally isolated marine Pseudomonas stutzeri MSEA04. Acta Biol Hung 67:305–317. https://doi.org/10.1556/018.67.2016.3.8
Bichara DA, Zhao X, Hwang NS et al (2010) Porous poly(vinyl alcohol)-alginate gel hybrid construct for neocartilage formation using human nasoseptal cells. J Surg Res 163:331–336. https://doi.org/10.1016/j.jss.2010.03.070
Boyd A, Ghosh M, May TB, Shinabarger D, Keogh R, Chakrabarty AM (1993) Sequence of the algL gene of Pseudomonas aeruginosa and purification of its alginate lyase product. Gene 131:1–8. https://doi.org/10.1016/0378-1119(93)90662-M
Brown BJ, Preston JF (1991) l-Guluronan-specific alginate lyase from a marine bacterium associated with Sargassum. Carbohydr Res 211:91–102. https://doi.org/10.1016/0008-6215(91)84148-84148
Bugli F, Posteraro B, Papi M, Torelli R, Maiorana A, Paroni Sterbini F, Posteraro P, Sanguinetti M, de Spirito M (2013) In vitro interaction between alginate lyase and amphotericin B against Aspergillus fumigatus biofilm determined by different methods. Antimicrob Agents Chemother 57:1275–1282. https://doi.org/10.1128/AAC.01875-12
Bugli F, Palmieri V, Torelli R et al (2016) In vitro effect of clarithromycin and alginate lyase against Helicobacter pylori biofilm. Biotechnol Prog 32:1584–1591. https://doi.org/10.1002/btpr.2339
Campbell KT, Stilhano RS, Silva EA (2018) Enzymatically degradable alginate hydrogel systems to deliver endothelial progenitor cells for potential revasculature applications. Biomaterials 179:109–121. https://doi.org/10.1016/j.biomaterials.2018.06.038
Chen XL, Dong S, Xu F et al (2016) Characterization of a new cold-adapted and salt-activated polysaccharide lyase family 7 alginate lyase from Pseudoalteromonas sp. SM0524. Front Microbiol 7:1–9. https://doi.org/10.3389/fmicb.2016.01120
Chen P, Zhu Y, Men Y et al (2018a) Purification and characterization of a novel alginate lyase from the marine bacterium Bacillus sp. Alg07. Mar Drugs 16:1–13. https://doi.org/10.3390/md16030086
Chen Y, Dou W, Li H, Shi J, Xu Z (2018b) the alginate lyase from Isoptericola halotolerans CGMCC 5336 as a new tool for the production of alginate oligosaccharides with guluronic acid as reducing end. Carbohydr Res 470:36–41. https://doi.org/10.1016/j.carres.2018.06.005
Cheng Y, Wang D, Gu J, Li J, Liu H, Li F, Han W (2017) Biochemical characteristics and variable alginate-degrading modes of a novel bifunctional endolytic alginate lyase. Appl Environ Microbiol 83:e01608–e01617. https://doi.org/10.1128/AEM.01608-17
Cho H, Huang X, Lan PY et al (2016) Molecular modeling and redesign of alginate lyase from Pseudomonas aeruginosa for accelerating CRPA biofilm degradation. Proteins Struct Funct Bioinforma 84:1875–1887. https://doi.org/10.1002/prot.25171
Cronan JE (2014) Escherichia coli as an experimental organism. In: eLS
Daboor SM, Raudonis R, Cohen A et al (2019) Marine bacteria, a source for alginolytic enzyme to disrupt Pseudomonas aeruginosa biofilms. Mar Drugs 17:307. https://doi.org/10.3390/md17050307
Eftekhar F, Schiller NL (1994) Partial purification and characterization of a mannuronan-specific alginate lyase from Pseudomonas aeruginosa. Curr Microbiol 29:37–42. https://doi.org/10.1007/BF01570189
Ertesvåg H (2015) Alginate-modifying enzymes: biological roles and biotechnological uses. Front Microbiol 6:1–10. https://doi.org/10.3389/fmicb.2015.00523
Ertesvåg H, Erlien F, Skjåk-Bræk G, Rehm BHA, Valla S (1998) Biochemical properties and substrate specificities of a recombinantly produced Azotobacter vinelandii alginate lyase. J Bacteriol 180:3779–3784
Fischer A, Wefers D (2019) Chromatographic analysis of alginate degradation by five recombinant alginate lyases from Cellulophaga algicola DSM 14237. Food Chem 299:125142. https://doi.org/10.1016/j.foodchem.2019.125142
Fu XT, Lin H, Kim SM (2007) Purification and characterization of a Na+/K+ dependent alginate lyase from turban shell gut Vibrio sp. YKW-34. Enzym Microb Technol 41:828–834. https://doi.org/10.1016/j.enzmictec.2007.07.003
Gacesa P (1992) Enzymic degradation of alginates. Int J BioChemiPhysics 24:545–552
Gacesa P, Wusteman FS (1990) Plate assay for simultaneous detection of alginate lyases and determination of substrate specificity. Appl Environ Microbiol 56:2265–2267
Ganjegunte G, Ulery A, Niu G, Wu Y (2017) Effects of treated municipal wastewater irrigation on soil properties, switchgrass biomass production and quality under arid climate. Ind Crop Prod 99:60–69. https://doi.org/10.1016/j.indcrop.2017.01.038
Gao S, Zhang Z, Li S, Su H, Tang L, Tan Y, Yu W, Han F (2018) Characterization of a new endo-type polysaccharide lyase (PL) family 6 alginate lyase with cold-adapted and metal ions-resisted property. Int J Biol Macromol 120:729–735. https://doi.org/10.1016/j.ijbiomac.2018.08.164
Garcia-Vaquero M, Rajauria G, O’Doherty JV, Sweeney T (2017) Polysaccharides from macroalgae: recent advances, innovative technologies and challenges in extraction and purification. Food Res Int 99:1011–1020. https://doi.org/10.1016/j.foodres.2016.11.016
Garron ML, Cygler M (2010) Structural and mechanistic classification of uronic acid-containing polysaccharide lyases. Glycobiology 20:1547–1573. https://doi.org/10.1093/glycob/cwq122
Garron ML, Cygler M (2014) Uronic polysaccharide degrading enzymes. Curr Opin Struct Biol 28:87–95. https://doi.org/10.1016/j.sbi.2014.07.012
Ghadam P, Akhlaghi F, Abdi Ali A (2017) One-step purification and characterization of alginate lyase from a clinical Pseudomonas aeruginosa with destructive activity on bacterial biofilm. Iran J Basic Med Sci 20:467–473. https://doi.org/10.22038/ijbms.2017.8668
Gimpel JA, Ravanal MC, Salazar O, Lienqueo ME (2018) Saccharification of brown macroalgae using an arsenal of recombinant alginate lyases: potential application in the biorefinery process. J Microbiol Biotechnol 28:1671–1682. https://doi.org/10.4014/jmb.1805.05056
Gomare S, Kim HA, Ha JH, Lee MW, Park JM (2011) Isolation of the polysaccharidase-producing bacteria from the gut of sea snail, Batillus cornutus. Korean J Chem Eng 28:1252–1259. https://doi.org/10.1007/s11814-010-0506-y
Gong JS, Liu XM, Zhang MJ et al (2017) Purification and characterization of a high salt-tolerant alginate lyase from Cobetia sp. WG-007. Biotechnol Appl Biochem 64:519–524. https://doi.org/10.1002/bab.1506
Han W, Gu J, Cheng Y, Liu H, Li Y, Li F (2016) Novel alginate lyase (Aly5) from a polysaccharide-degrading marine bacterium, Flammeovirga sp. strain MY04: effects of module truncation on biochemical characteristics, alginate degradation patterns, and oligosaccharide-yielding properties. Appl Environ Microbiol 82:364–374. https://doi.org/10.1128/AEM.03022-15
Hashimoto W, Miyake O, Ochiai A, Murata K (2005) Molecular identification of Sphingomonas sp. A1 alginate lyase (A1-IV′) as a member of novel polysaccharide lyase family 15 and implications in alginate lyase evolution. J Biosci Bioeng 99:48–54. https://doi.org/10.1263/jbb.99.48
Hatanaka C, Kobara Y (1980) Determination of glucose by a modification of Somogyi-Nelson method. Agric Biol Chem 44:2943–2949. https://doi.org/10.1271/bbb1961.44.2943
He M, Guo M, Zhang X et al (2018) Purification and characterization of alginate lyase from Sphingomonas sp. ZH0. J Biosci Bioeng 126:310–316. https://doi.org/10.1016/j.jbiosc.2018.01.017
Hirayama M, Hashimoto W, Murata K, Kawai S (2016) Comparative characterization of three bacterial exo-type alginate lyases. Int J Biol Macromol 86:519–524. https://doi.org/10.1016/j.ijbiomac.2016.01.095
Hu X, Jiang X, Hwang H, Liu S, Gua H (2004) Antitumour activities of alginate-derived oligosaccharides and their sulphated substitution derivatives. Eur J Phycol 39:67–71. https://doi.org/10.1080/09670260310001636695
Hu X, Jiang X, Hwang HM (2006) Purification and characterization of an alginate lyase from marine bacterium Vibrio sp. mutant strain 510-64. Curr Microbiol 53:135–140. https://doi.org/10.1007/s00284-005-0347-9
Huang W, Matte A, Li Y, Kim YS, Linhardt RJ, Su H, Cygler M (1999) Crystal structure of chondroitinase B from Flavobacterium heparinum and its complex with a disaccharide product at 1.7 Å resolution. J Mol Biol 294:1257–1269. https://doi.org/10.1006/jmbi.1999.3292
Huang L, Zhou J, Li X et al (2013) Characterization of a new alginate lyase from newly isolated Flavobacterium sp. S20. J Ind Microbiol Biotechnol 40:113–122. https://doi.org/10.1007/s10295-012-1210-1
Huang G, Wang Q, Lu M, Xu C, Li F, Zhang R, Liao W, Huang S (2018) AlgM4: a new salt-activated alginate lyase of the PL7 family with endolytic activity. Mar Drugs 16:120. https://doi.org/10.3390/md16040120
Huang G, Wen S, Liao S et al (2019) Characterization of a bifunctional alginate lyase as a new member of the polysaccharide lyase family 17 from a marine strain BP-2. Biotechnol Lett 41:1187–1200. https://doi.org/10.1007/s10529-019-02722-1
Hunt NC, Hallam D, Karimi A, Mellough CB, Chen J, Steel DHW, Lako M (2017) 3D culture of human pluripotent stem cells in RGD-alginate hydrogel improves retinal tissue development. Acta Biomater 49:329–343. https://doi.org/10.1016/j.actbio.2016.11.016
Iehata S, Inagaki T, Okunishi S, Nakano M, Tanaka R, Maeda H (2010) Improved gut environment of abalone Haliotis gigantea through Pediococcus sp. Ab1 treatment. Aquaculture 305:59–65. https://doi.org/10.1016/j.aquaculture.2010.04.012
In Lee S, Choi SH, Lee EY, Kim HS (2012) Molecular cloning, purification, and characterization of a novel polyMG-specific alginate lyase responsible for alginate MG block degradation in Stenotrophomas maltophilia KJ-2. Appl Microbiol Biotechnol 95:1643–1653. https://doi.org/10.1007/s00253-012-4266-y
Inoue A, Ojima T (2019) Functional identification of alginate lyase from the brown alga Saccharina japonica. Sci Rep 9:11. https://doi.org/10.1038/s41598-019-41351-6
Inoue A, Takadono K, Nishiyama R, Tajima K, Kobayashi T, Ojima T (2014) Characterization of an alginate lyase, FlAlyA, from Flavobacterium sp. strain UMI-01 and its expression in Escherichia coli. Mar Drugs 12:4693–4712. https://doi.org/10.3390/md12084693
Inoue A, Mashino C, Uji T, Saga N, Mikami K, Ojima T (2015) Characterization of an eukaryotic PL-7 alginate lyase in the marine red alga Pyropia yezoensis. Curr Biotechnol 4:240–258. https://doi.org/10.2174/2211550104666150915210434
Inoue A, Anraku M, Nakagawa S, Ojima T (2016) Discovery of a novel alginate lyase from Nitratiruptor sp. SB155-2 thriving at deep-sea hydrothermal vents and identification of the residues responsible for its heat stability. J Biol Chem 291:1551–15563. https://doi.org/10.1074/jbc.M115.713230
Islan GA, Bosio VE, Castro GR (2013) Alginate lyase and ciprofloxacin co-immobilization on biopolymeric microspheres for cystic fibrosis treatment. Macromol Biosci 13:1238–1248. https://doi.org/10.1002/mabi.201300134
Itoh T, Nakagawa E, Yoda M, Nakaichi A, Hibi T, Kimoto H (2019) Structural and biochemical characterization of a novel alginate lyase from Paenibacillus sp. str. FPU-7. Sci Rep 9:1–14. https://doi.org/10.1038/s41598-019-51006-1
Iwamoto Y, Araki R, Iriyama KI et al (2001) Purification and characterization of bifunctional alginate lyase from Alteromonas sp. strain no. 272 and its action on saturated oligomeric substrates. Biosci Biotechnol Biochem 65:133–142. https://doi.org/10.1271/bbb.65.133
Jang CH, Piao YL, Huang X, Yoon EJ, Park SH, Lee K, Zhan CG, Cho H (2016) Modeling and re-engineering of Azotobacter vinelandii alginate lyase to enhance its catalytic efficiency for accelerating biofilm degradation. PLoS One 11:e0156197. https://doi.org/10.1371/journal.pone.0156197
Ji S, Dix SR, Aziz AA, Sedelnikova SE, Baker PJ, Rafferty JB, Bullough PA, Tzokov SB, Agirre J, Li FL, Rice DW (2019) the molecular basis of endolytic activity of a multidomain alginate lyase from Defluviitalea phaphyphila, a representative of a new lyase family, PL39. J Biol Chem 294:18077–18091. https://doi.org/10.1074/jbc.RA119.010716
Jiang Z, Guo Y, Wang X, Li H, Ni H, Li L, Xiao A, Zhu Y (2019) Molecular cloning and characterization of AlgL17, a new exo-oligoalginate lyase from Microbulbifer sp. ALW1. Protein Expr Purif 161:17–27. https://doi.org/10.1016/j.pep.2019.03.015
John RP, Anisha GS, Nampoothiri KM, Pandey A (2011) Micro and macroalgal biomass: a renewable source for bioethanol. Bioresour Technol 102:186–193. https://doi.org/10.1016/j.biortech.2010.06.139
Kennedy JF, barnes BA, barker SA (1983) the use of alginate ester films on solid supports in the preparation of water-insoluble immunoadsorbents for purification of antigens. Eur J Biochem 133:697–705. https://doi.org/10.1111/j.1432-1033.1983.tb07519.x
Kennedy L, McDowell K, Sutherland IW (1992) Alginases from Azotobacter species. J Gen Microbiol 138:2465–2471. https://doi.org/10.1099/00221287-138-11-2465
Khan S, Tøndervik A, Sletta H, Klinkenberg G, Emanuel C, Onsøyen E, Myrvold R, Howe RA, Walsh TR, Hill KE, Thomas DW (2012) Overcoming drug resistance with alginate oligosaccharides able to potentiate the action of selected antibiotics. Antimicrob Agents Chemother 56:5134–5141. https://doi.org/10.1128/AAC.00525-12
Kim DE, Lee EY, Kim HS (2009) Cloning and characterization of alginate lyase from a marine bacterium Streptomyces sp. ALG-5. Mar Biotechnol 11:10. https://doi.org/10.1007/s10126-008-9114-9
Kim D, Baik KS, Hwang YS, Choi JS, Kwon J, Seong CN (2013a) Vibrio hemicentroti sp. nov., an alginate lyase-producing bacterium, isolated from the gut microflora of sea urchin (Hemicentrotus pulcherrimus). Int J Syst Evol Microbiol 63:3697–3703. https://doi.org/10.1099/ijs.0.047951-0
Kim EJ, Fathoni A, Jeong GT et al (2013b) Microbacterium oxydans, a novel alginate- and laminarin-degrading bacterium for the reutilization of brown-seaweed waste. J Environ Manag 130:153–159. https://doi.org/10.1016/j.jenvman.2013.08.064
Kitamikado M, Tseng CH, Yamaguchi K, Nakamura T (1992) Two types of bacterial alginate lyases. Appl Environ Microbiol 58:2474–2478
Kleinschmidt K, Klinge PM, Stopa E et al (2011) Alginate encapsulated human mesenchymal stem cells suppress syngeneic glioma growth in the immunocompetent rat. J Microencapsul 28:621–627. https://doi.org/10.3109/02652048.2011.599441
Kunjukunju S, Roy A, Shekhar S, Kumta PN (2018) Cross-linked enzyme aggregates of alginate lyase: a systematic engineered approach to controlled degradation of alginate hydrogel. Int J Biol Macromol 115:176–184. https://doi.org/10.1016/j.ijbiomac.2018.03.110
Kurakake M, Kitagawa Y, Okazaki A, Shimizu K (2017) Enzymatic properties of alginate lyase from Paenibacillus sp. S29. Appl Biochem Biotechnol 183:1455–1464. https://doi.org/10.1007/s12010-017-2513-5
Li L, Jiang X, Gua H, Wang P (2011) Preparation, purification and characterization of alginate oligosaccharides degraded by alginate lyase from Pseudomonas sp. HZJ 216. Carbohydr Res 346:794–800. https://doi.org/10.1016/j.carres.2011.01.023
Li S, Yang X, Zhang L et al (2015) Cloning, expression, and characterization of a cold-adapted and surfactant-stable alginate lyase from marine bacterium Agarivorans sp. L11. J Microbiol Biotechnol 25:681–686. https://doi.org/10.4014/jmb.1409.09031
Li M, Li G, Shang Q, Chen X, Liu W, Pi X', Zhu L, Yin Y, Yu G, Wang X (2016) In vitro fermentation of alginate and its derivatives by human gut microbiota. Anaerobe 39:19–25. https://doi.org/10.1016/j.anaerobe.2016.02.003
Li M, Shang Q, Li G, Wang X, Yu G (2017a) Degradation of marine algae-derived carbohydrates by Bacteroidetes isolated from human gut microbiota. Mar Drugs 15:92. https://doi.org/10.3390/md15040092
Li S, Wang L, Hao J et al (2017b) Purification and characterization of a new alginate lyase from marine bacterium Vibrio sp. SY08. Mar Drugs 15:1. https://doi.org/10.3390/md15010001
Li H, Wang S, Zhang Y, Chen L (2018) High-level expression of a thermally stable alginate lyase using Pichia pastoris, characterization and application in producing brown alginate oligosaccharide. Mar Drugs 16:158. https://doi.org/10.3390/md16050158
Li Q, Hu F, Zhu B et al (2019) Biochemical characterization and elucidation of action pattern of a novel polysaccharide lyase 6 family alginate lyase from marine bacterium Flammeovirga sp. nj-04. Mar Drugs 17:323. https://doi.org/10.3390/md17060323
Lin JD, Lemay MA, Parfrey LW (2018) Diverse bacteria utilize alginate wifin the microbiome of the giant kelp Macrocystis pyrifera. Front Microbiol 9:1914. https://doi.org/10.3389/fmicb.2018.01914
Liu J, Yang S, Li X, Yan Q, Reaney MJT, Jiang Z (2019) Alginate oligosaccharides: production, biological activities, and potential applications. Compr Rev Food Sci Food Saf 18:1859–1881. https://doi.org/10.1111/1541-4337.12494
MacDonald LC, Berger BW (2014) A polysaccharide lyase from Stenotrophomonas maltophilia with a unique, pH-regulated substrate specificity. J Biol Chem 289:312–325. https://doi.org/10.1074/jbc.M113.489195
Mackie W (1971) Conformations of crystalline alginic acids and their salts. Biochem J 125:950. https://doi.org/10.1042/bj1250089pa
Malissard M, Chavagnat F, Duez C et al (1995) Overproduction and properties of the mannuronate alginate lyase AlxMB. FEMS Microbiol Lett 126:105–111. https://doi.org/10.1016/0378-1097(94)00536-Z
Markstedt K, Mantas A, Tournier me, Martínez Ávila H, Hägg D, Gatenholm P (2015) 3D bioprinting human chondrocytes with nanocellulose-alginate bioink for cartilage tissue engineering applications. Biomacromolecules 16:1489–1496. https://doi.org/10.1021/acs.biomac.5b00188
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 6:1–14. https://doi.org/10.3389/fmicb.2015.01487
Matsubara Y, Yusa T, Sawabe A, Iizuka Y, Okamoto K (1991) Structure and physiological activity of phenyl propanoid glycosides in lemon (Citrus limon BURM. f.) peel. Agric Biol Chem 55:647–650. https://doi.org/10.1080/00021369.1991.10870631
McHugh D (2003) A guide to the seaweed industry: FAO fisheries technical paper 441. Rome
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
Mohapatra BR (2017) Kinetic and thermodynamic properties of alginate lyase and cellulase co-produced by Exiguobacterium species Alg-S5. Int J Biol Macromol 98:103–110. https://doi.org/10.1016/j.ijbiomac.2017.01.091
Mori T, Takahashi M, Tanaka R, Miyake H, Shibata T, Chow S, Kuroda K, Ueda M, Takeyama H (2016) Falsirhodobacter sp. alg1 harbors single homologs of endo and exo-type alginate lyases efficient for alginate depolymerization. PLoS One 11:1–16. https://doi.org/10.1371/journal.pone.0155537
Negro MJ, Manzanares P, Ballesteros I et al (2003) Hydrothermal pretreatment conditions to enhance ethanol production from poplar biomass. Appl Biochem Biotechnol 105-108:87–100. https://doi.org/10.1385/ABAB:105:1-3:87
Ochiai A, Yamasaki M, Mikami B, Hashimoto W, Murata K (2010) Crystal structure of exotype alginate lyase Atu3025 from Agrobacterium tumefaciens. J Biol Chem 285(32):24519–24528. https://doi.org/10.1074/jbc.M110.125450
Østgaard K, Knutsen SH, Dyrset N, Aasen IM (1993) Production and characterization of guluronate lyase from Klebsiella pneumoniae for applications in seaweed biotechnology. Enzym Microb Technol 15:756–763. https://doi.org/10.1016/0141-0229(93)90006-N
Pacaldo RS, Volk TA, Briggs RD (2013) Greenhouse gas potentials of shrub willow biomass crops based on below- and aboveground biomass inventory along a 19-year chronosequence. Bioenergy Res 6:252–262. https://doi.org/10.1007/s12155-012-9250-y
Patel KK, Tripathi M, Pandey N, Agrawal AK, Gade S, Anjum MM, Tilak R, Singh S (2019) Alginate lyase immobilized chitosan nanoparticles of ciprofloxacin for the improved antimicrobial activity against the biofilm associated mucoid P. aeruginosa infection in cystic fibrosis. Int J Pharm 563:30–42. https://doi.org/10.1016/j.ijpharm.2019.03.051
Peciña A, Pascual A, Paneque A (1999) Cloning and expression of the algL gene, encoding the Azotobacter chroococcum alginate lyase: purification and characterization of the enzyme. J Bacteriol 181:1409–1414
Pei X, Chang Y, Shen J (2019) Cloning, expression, and characterization of an endo-acting bifunctional alginate lyase of marine bacterium Wenyingzhuangia fucanilytica. Protein Expr Purif 154:44–51. https://doi.org/10.1016/j.pep.2018.09.010
Peng C, Wang Q, Lu D et al (2018) A novel bifunctional endolytic alginate lyase with variable alginate-degrading modes and versatile monosaccharide-producing properties. Front Microbiol 9:167. https://doi.org/10.3389/fmicb.2018.00167
Petzold G, Rodríguez A, Valenzuela R et al (2019) Alginate as a versatile polymer matrix with biomedical and food applications. Mater Biomed Eng 323–350. https://doi.org/10.1016/b978-0-12-818415-8.00012-7
Pilgaard B, Wilkens C, Herbst FA, Vuillemin M, Rhein-Knudsen N, Meyer AS, Lange L (2019) Proteomic enzyme analysis of the marine fungus Paradendryphiella salina reveals alginate lyase as a minimal adaptation strategy for brown algae degradation. Sci Rep 9:1–3. https://doi.org/10.1038/s41598-019-48823-9
Qin Y (2008) Alginate fibres: an overview of the production processes and applications in wound management. Polym Int 57:171–180. https://doi.org/10.1002/pi.2296
Qin HM, Miyakawa T, Inoue A, Nishiyama R, Nakamura A, Asano A, Ojima T, Tanokura M (2018) Structural basis for controlling the enzymatic properties of polymannuronate preferred alginate lyase FlAlyA from the PL-7 family. Chem Commun 54:555–558. https://doi.org/10.1039/c7cc06523j
Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ Jr, Hallett JP, Leak DJ, Liotta CL, Mielenz JR, Murphy R, ler R, Tschaplinski T (2006) The path forward for biofuels and biomaterials. Science 311:484–489. https://doi.org/10.1126/science.1114736
Remminghorst U, Rehm BHA (2006) Bacterial alginates: from biosynthesis to applications. Biotechnol Lett 28(21):1701–1712. https://doi.org/10.1007/s10529-006-9156-x
Sato R, Katayama S, Sawabe T, Saeki H (2003) Stability and emulsion-forming ability of water-soluble fish myofibrillar protein prepared by conjugation with alginate oligosaccharide. J Agric Food Chem 51:4376–4381. https://doi.org/10.1021/jf021023v
Sawant SS, Salunke BK, Kim BS (2015) A rapid, sensitive, simple plate assay for detection of microbial alginate lyase activity. Enzym Microb Technol 77:8–13. https://doi.org/10.1016/j.enzmictec.2015.05.003
Shin JW, Lee OK, Park HH et al (2015) Molecular characterization of a novel oligoalginate lyase consisting of AlgL- and heparinase II / III-like domains from Stenotrophomonas maltophilia KJ-2 and its application to alginate saccharification. 32:917–924. https://doi.org/10.1007/s11814-014-0282-1
Sim SJ, Baik KS, Park SC, Choe HN, Seong CN, Shin TS, Woo HC, Cho JY, Kim D (2012) Characterization of alginate lyase gene using a metagenomic library constructed from the gut microflora of abalone. J Ind Microbiol Biotechnol 39:585–593. https://doi.org/10.1007/s10295-011-1054-0
Stender EGP, Dybdahl Andersen C, Fredslund F, Holck J, Solberg A, Teze D, Peters GHJ, Christensen BE, Aachmann FL, Welner DH, Svensson B (2019) Structural and functional aspects of mannuronic acid specific PL6 alginate lyase from the human gut microbe Bacteroides cellulosilyticus. J Biol Chem 294:17915–17930. https://doi.org/10.1074/jbc.ra119.010206
Sun X, Shen W, Gao Y et al (2019) Heterologous expression and purification of a marine alginate lyase in Escherichia coli. Protein Expr Purif 153:97–104. https://doi.org/10.1016/j.pep.2018.09.002
Swift SM, Hudgens JW, Heselpoth RD et al (2014) Characterization of AlgMsp, an alginate lyase from Microbulbifer sp. 6532A. PLoS One 9. https://doi.org/10.1371/journal.pone.0112939
Tavafi H, Abdi-Ali A, Ghadam P, Gharavi S (2017) Screening of alginate lyase-producing bacteria and optimization of media compositions for extracellular alginate Lyase production. Iran Biomed J 21:48–56. https://doi.org/10.18869/acadpub.ibj.21.1.48
Tavafi H, Ali AA, Ghadam P, Gharavi S (2018) Screening, cloning and expression of a novel alginate lyase gene from P. aeruginosa TAG 48 and its antibiofilm effects on P. aeruginosa biofilm. Microb Pathog 124:356–364. https://doi.org/10.1016/j.micpath.2018.08.018
Tomoda Y, Umemura K, Adachi T (1994) Promotion of barley root elongation under hypoxic conditions by alginate lyase-lysate (ALL). Biosci Biotechnol Biochem 58:202–203. https://doi.org/10.1271/bbb.58.202
Tøndervik A, Sletta H, Klinkenberg G et al (2014) Alginate oligosaccharides inhibit fungal cell growth and potentiate the activity of antifungals against Candida and Aspergillus sp. PLoS One 9. https://doi.org/10.1371/journal.pone.0112518
Tønnesen HH, Karlsen J (2002) Alginate in drug delivery systems. Drug Dev Ind Pharm 28:621–630. https://doi.org/10.1081/ddc-120003853
Vuoristo KS, Fredriksen L, Oftebro M, Arntzen MØ, Aarstad OA, Stokke R, Steen IH, Hansen LD, Schüller RB, Aachmann FL, Horn SJ, Eijsink VGH (2019) Production, characterization, and application of an alginate lyase, AMOR-PL7A, from hot vents in the Arctic Mid-Ocean Ridge. J Agric Food Chem 67:2936–2945. https://doi.org/10.1021/acs.jafc.8b07190
Wang YH, Guang-Li Y, Wang XM et al (2006) Purification and characterization of alginate lyase from marine Vibrio sp. YWA. Acta Biochim Biophys Sin 38:633–638. https://doi.org/10.1111/j.1745-7270.2006.00210.x
Wang DM, Kim HT, Yun EJ, Kim DH, Park YC, Woo HC, Kim KH (2014) Optimal production of 4-deoxy-l-erythro-5-hexoseulose uronic acid from alginate for brown macro algae saccharification by combining endo- and exo-type alginate lyases. Bioprocess Biosyst Eng 37:2105–2111. https://doi.org/10.1007/s00449-014-1188-3
Wang L, Li S, Yu W, Gong Q (2015) Cloning, overexpression, and characterization of a new oligoalginate lyase from a marine bacterium, Shewanella sp. Biotechnol Lett 37:665–671. https://doi.org/10.1007/s10529-014-1706-z
Wang M, Chen L, Liu Z et al (2016) Isolation of a novel alginate lyase-producing Bacillus litoralis strain and its potential to ferment Sargassum horneri for biofertilizer. Microbiologyopen 5:1038–1049. https://doi.org/10.1002/mbo3.387
Wang D, Aarstad OA, Li J, McKee LS, Sætrom GI, Vyas A, Srivastava V, Aachmann FL, Bulone V, Hsieh YSY (2018) Preparation of 4-Deoxy- L -erythro-5-hexoseulose uronic acid (DEH) and guluronic acid rich alginate using a unique exo-alginate lyase from Thalassotalea crassostreae. J Agric Food Chem 66:1435–1443. https://doi.org/10.1021/acs.jafc.7b05751
Wang Y, Chen X, Bi X, Ren Y, Han Q, Zhou Y, Han Y, Yao R, Li S (2019) Characterization of an alkaline alginate lyase with pH-stable and thermo-tolerance property. Mar Drugs 17:1–14. https://doi.org/10.3390/md17050308
Wintter JE, Lauter WM, Foote PA (1955) Derivatives of alginic acid. J Am Pharm Assoc Am Pharm Assoc (Baltim) 44:48–51. https://doi.org/10.1002/jps.3030440118
Wong TY, Preston LA, Schiller NL (2000) Alginate lyase: review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annu Rev Microbiol 54:289–340. https://doi.org/10.1146/annurev.micro.54.1.289
Woodard KR, Prine GM, Bates DB, Chynoweth DP (1991) Preserving elephantgrass and energycane biomass as silage for energy. Bioresour Technol 36:253–259. https://doi.org/10.1016/0960-8524(91)90232-9
Xiao L, Han F, Yang Z, Lu XZ, Yu WG (2006) A novel alginate lyase with high activity on acetylated alginate of Pseudomonas aeruginosa FRD1 from Pseudomonas sp. QD03. World J Microbiol Biotechnol 22:81–88. https://doi.org/10.1007/s11274-005-7713-4
Xu F, Dong F, Wang P, Cao HY, Li CY, Li PY, Pang XH, Zhang YZ, Chen XL (2017) Novel molecular insights into the catalytic mechanism of marine bacterial alginate lyase AlyGC from polysaccharide lyase family 6. J Biol Chem 292:4457–4468. https://doi.org/10.1074/jbc.M116.766030
Xu F, Wang P, Zhang YZ, Chen XL (2018) Diversity of three-dimensional structures and catalytic mechanisms of alginate lyases. Appl Environ Microbiol 84:1–12. https://doi.org/10.1128/AEM.02040-17
Xue X, Zhou Y, Gao X, Yan P (2019) Advances in application of alginate lyase and its enzymatic hydrolysate. In: IOP Conference Series: Materials Science and Engineering 612:022005. https://doi.org/10.1088/1757-899X/612/2/022005
Yagi H, Fujise A, Itabashi N, Ohshiro T (2016) Purification and characterization of a novel alginate lyase from the marine bacterium Cobetia sp. NAP1 isolated from brown algae. Biosci Biotechnol Biochem 80:2338–2346. https://doi.org/10.1080/09168451.2016.1232154
Yagi H, Fujise A, Itabashi N, Ohshiro T (2018a) Characterization of a novel endo-type alginate lyase derived from Shewanella sp. YH1. J Biochem 163:341–350. https://doi.org/10.1093/jb/mvy001
Yagi H, Isobe N, Itabashi N, Fujise A, Ohshiro T (2018b) Characterization of a long-lived alginate lyase derived from Shewanella species YH1. Mar Drugs 16:4. https://doi.org/10.3390/md16010004
Yan J, Chen P, Zeng Y et al (2019) the characterization and modification of a novel bifunctional and robust alginate lyase derived from Marinimicrobium sp. H1. Mar Drugs 17:545. https://doi.org/10.3390/md17100545
Yang X, Li S, Wu Y et al (2016) Cloning and characterization of two thermo- and salt-tolerant oligoalginate lyases from marine bacterium Halomonas sp. FEMS Microbiol Lett 363:fnw079. https://doi.org/10.1093/femsle/fnw079
Yang M, Yu Y, Yang S et al (2018) Expression and characterization of a new polyg-specific alginate lyase from marine bacterium Microbulbifer sp. Q7. Front Microbiol 9:2894. https://doi.org/10.3389/fmicb.2018.02894
Yang M, Yang SX, Liu ZM et al (2019) Rational design of alginate lyase from Microbulbifer sp. Q7 to improve thermal stability. Mar Drugs 17:378. https://doi.org/10.3390/md17060378
Yokose T, Nishikawa T, Yamamoto Y et al (2009) Growth-promoting effect of alginate oligosaccharides on a unicellular marine microalga, nannochloropsis oculata. Biosci Biotechnol Biochem 73:450–453. https://doi.org/10.1271/bbb.80692
Yonemoto Y, Murata K, Kimura A, Yamaguchi H, Okayama K (1991) Bacterial alginate lyase: characterization of alginate lyase-producing bacteria and purification of the enzyme. J Ferment Bioeng 72:152–157. https://doi.org/10.1016/0922-338X(91)90208-X
Yoon HJ, Mikami B, Hashimoto W, Murata K (1999) Crystal structure of alginate lyase A1-III from Sphingomonas species A1 at 1.78 Å resolution. J Mol Biol 290:505–514. https://doi.org/10.1006/jmbi.1999.2883
Yu Z, Zhu B, Wang W, Ta H, Yin H (2018) Characterization of a new oligoalginate lyase from marine bacterium Vibrio sp. Int J Biol Macromol 112:937–942. https://doi.org/10.1016/j.ijbiomac.2018.02.046
Yue MM, Gong WW, Qiao Y, Ding H (2016) A method for efficient expression of Pseudomonas aeruginosa alginate lyase in Pichia pastoris. Prep Biochem Biotechnol 46:165–170. https://doi.org/10.1080/10826068.2014.996233
Zeng J, An D, Jiao C, Xiao Q, Weng H, Yang Q, Xiao A (2019) Cloning, expression, and characterization of a new pH- and heat-stable alginate lyase from Pseudoalteromonas carrageenovora ASY5. J Food Biochem 43:e12886. https://doi.org/10.1111/jfbc.12886
Zhu B, Yin H (2015) Alginate lyase: review of major sources and classification, properties, structure-function analysis, and applications. Bioengineered 6:125–131. https://doi.org/10.1080/21655979.2015.1030543
Zhu BW, Huang LSX, Tan HD, Qin YQ, du YG, Yin H (2015) Characterization of a new endo-type polyM-specific alginate lyase from Pseudomonas sp. Biotechnol Lett 37:409–415. https://doi.org/10.1007/s10529-014-1685-0
Zhu B, Chen M, Yin H et al (2016a) Enzymatic hydrolysis of alginate to produce oligosaccharides by a new purified endo-type alginate lyase. Mar Drugs 14:108. https://doi.org/10.3390/md14060108
Zhu Y, Wu L, Chen Y, Ni H, Xiao A, Cai H (2016b) Characterization of an extracellular bifunctional alginate lyase from marine Microbulbifer sp. ALW1 and antioxidant activity of enzymatic hydrolysates. Microbiol Res 182:49–58. https://doi.org/10.1016/j.micres.2015.09.004
Zhu B, Ni F, Sun Y, Yao Z (2017) Expression and characterization of a new heat-stable endo-type alginate lyase from deep-sea bacterium Flammeovirga sp. NJ-04. Extremophiles 21:1027–1036. https://doi.org/10.1007/s00792-017-0962-y
Zhu B, Hu F, Yua H et al (2018a) Biochemical characterization and degradation pattern of a unique pH-stable PolyM-specific alginate lyase from newly isolated Serratia marcescens NJ-07. Mar Drugs 16:129. https://doi.org/10.3390/md16040129
Zhu B, Ni F, Ning L, Sun Y, Yao Z (2018b) Cloning and characterization of a new pH-stable alginate lyase with high salt tolerance from marine Vibrio sp. NJ-04. Int J Biol Macromol 115:1063–1070. https://doi.org/10.1016/j.ijbiomac.2018.04.108
Zhu B, Ning L, Jiang Y, Ge L (2018c) Biochemical characterization and degradation pattern of a novel endo-type bifunctional alginate lyase AlyA from marine bacterium Isoptericola halotolerans. Mar Drugs 16:258. https://doi.org/10.3390/md16080258
Zhu B, Sun Y, Ni F, Ning L, Yao Z (2018d) Characterization of a new endo-type alginate lyase from Vibrio sp. NJU-03. Int J Biol Macromol 108:1140–1147. https://doi.org/10.1016/j.ijbiomac.2017.10.164
Zhu X, Li X, Shi H et al (2018e) Characterization of a novel alginate lyase from marine bacterium Vibrio furnissii H1. Mar Drugs 16:30. https://doi.org/10.3390/md16010030
Zhu B, Li K, Wang W et al (2019a) Preparation of trisaccharide from alginate by a novel alginate lyase Alg7A from marine bacterium Vibrio sp. W13. Int J Biol Macromol 139:879–885. https://doi.org/10.1016/j.ijbiomac.2019.08.020
Zhu B, Ni F, Sun Y, Ning L, Yao Z (2019b) Elucidation of degrading pattern and substrate recognition of a novel bifunctional alginate lyase from Flammeovirga sp. NJ-04 and its use for preparation alginate oligosaccharides. Biotechnol Biofuels 12:1–3. https://doi.org/10.1186/s13068-019-1352-8
Zhuang J, Zhang K, Liu X, Liu W, Lyu Q, Ji A (2018) Characterization of a novel polyM-preferred alginate lyase from marine Vibrio splendidus OU02. Mar Drugs 16:295. https://doi.org/10.3390/md16090295
Zilda DS, Yulianti Y, Sholihah RF et al (2019) A novel Bacillus sp. isolated from rotten seaweed: identification and characterization alginate lyase its produced Biodiversitas 20:1166–1172. https://doi.org/10.13057/biodiv/d200432
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We would like to acnoledge the research support of SRM Institute of Science and Technology, Kattankulathur - 603203, India.
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Dharani, S.R., Srinivasan, R., Sarath, R. et al. Recent progress on engineering microbial alginate lyases towards their versatile role in biotechnological applications. Folia Microbiol 65, 937–954 (2020). https://doi.org/10.1007/s12223-020-00802-8
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DOI: https://doi.org/10.1007/s12223-020-00802-8