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Agar degradation by microorganisms and agar-degrading enzymes

Applied Microbiology and Biotechnology volume 94, pages 917–930 (2012)Cite this article

Abstract

Agar is a mixture of heterogeneous galactans, mainly composed of 3,6-anhydro-l-galactoses (or l-galactose-6-sulfates) d-galactoses and l-galactoses (routinely in the forms of 3,6-anhydro-l-galactoses or l-galactose-6-sulfates) alternately linked by β-(1,4) and α-(1,3) linkages. It is a major component of the cell walls of red algae and has been used in a variety of laboratory and industrial applications, owing to its jellifying properties. Many microorganisms that can hydrolyze and metabolize agar as a carbon and energy source have been identified in seawater and marine sediments. Agarolytic microorganisms commonly produce agarases, which catalyze the hydrolysis of agar. Numerous agarases have been identified in microorganisms of various genera. They are classified according to their cleavage pattern into three types—α-agarase, β-agarase, and β-porphyranase. Although, in a broad sense, many other agarases are involved in complete hydrolysis of agar, most of those identified are β-agarases. In this article we review agarolytic microorganisms and their agar-hydrolyzing systems, covering β-agarases as well as α-agarases, α-neoagarobiose hydrolases, and β-porphyranases, with emphasis on the recent discoveries. We also present an overview of the biochemical and structural characteristics of the various types of agarases. Further, we summarize and compare the agar-hydrolyzing systems of two specific microorganisms: Gram-negative Saccharophagus degradans 2–40 and Gram-positive Streptomyces coelicolor A3(2). We conclude with a brief discussion of the importance of agarases and their possible future application in producing oligosaccharides with various nutraceutical activities and in sustainably generating stock chemicals for biorefinement and bioenergy.

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References

  • Allouch J, Helbert W, Henrissat B, Czjzek M (2004) Parallel substrate binding sites in a beta-agarase suggest a novel mode of action on double-helical agarose. Structure 12:623–632

    CAS  Google Scholar 

  • Allouch J, Jam M, Helbert W, Barbeyron T, Kloareg B, Henrissat B, Czjzek M (2003) The three dimensional structures of two beta agarases. J Biol Chem 278:47171–47180

    Article  CAS  Google Scholar 

  • Andrykovitch G, Marx I (1988) Isolation of a new polysaccharide-digesting bacterium from a salt marsh. Appl Environ Microbiol 54:3–4

    Google Scholar 

  • Araki C (1959) Seaweed polysaccharides. In: Wolfrom ML (ed) Carbohydrate chemistry of substances of biological interest. Pergamon, London, pp 15–30

    Google Scholar 

  • Araki T, Hayakawa M, Lu Z, Karita S, Morishita T (1998) Purification and characterization of agarases from a marine bacterium, Vibrio sp. PO-303. J Mar Biotechnol 6:260–265

    Google Scholar 

  • Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782–791

    Article  CAS  Google Scholar 

  • Barbeyron T, L’Haridon S, Corre E, Kloareg B, Potin P (2001) Zobellia galactanovorans gen. nov., sp. nov., a marine species of Flavobacterlaceae isolated from a red alga, and classification of [Cytophaga] uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Zobellia uliginosa gen. nov., comb. nov. Int J Syst Evol Microbiol 51:985–997

    Article  CAS  Google Scholar 

  • Barbeyron T, Potin P, Richard C, Collin O, Kloareg B (1995) Arylsulphatase from Alteromonas carrageenovora. Microbiology 141:2897–2904

    Article  CAS  Google Scholar 

  • Bentley SD, Chater KF, Cerdeño-Tárraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O'Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147

    Article  Google Scholar 

  • Bibb MJ, Jones GH, Joseph R, Buttner MJ, Ward JM (1987) The agarase gene (dagA) of Streptomyces coelicolor A3(2): affinity purification and characterization of the cloned gene product. J Gen Microbiol 133:2089–2096

    CAS  Google Scholar 

  • Boraston A, Bolam D, Gilbert H, Davies G (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781

    Article  CAS  Google Scholar 

  • Buttner MJ, Fearnley JM, Bibb MJ (1987) The agarase gene (dagA) of Streptomyces coelicolor A3(2): nucleotide sequence and transcriptional analysis. Mol Gen Genet 209:101–109

    Article  CAS  Google Scholar 

  • Buttner MJ, Smith AM, Bibb MJ (1988) At least three different RNA polymerase holoenzymes direct transcription of the agarase gene (dagA) of Streptomyces coelicolor A3(2). Cell 52:599–607

    Article  CAS  Google Scholar 

  • Carlsson U, Ferskgård PO, Svensson SC (1991) A simple and efficient synthesis of the inducer IPTG made for inexpensive heterologous protein production using the lac-promoter. Protein Eng 4:1019–1020

    Article  CAS  Google Scholar 

  • Cho ES, Kim JH, Kim YH, Nam SW (2010) Characterization of agarose produced by yeast cell surface displayed-arylsulfatase. Kor J Microbiol Biotechnol 38:428–433

    CAS  Google Scholar 

  • Correc G, Hehemann J-H, Czjzek M, Helbert W (2011) Structural analysis of the degradation products of porphyran digested by Zobellia galactanivorans β-porphyranase A. Carbohydr Polym 83:277–283

    Google Scholar 

  • d’Enfert C, Ryter A, Pugsley AP (1987) Cloning and expression in Escherichia coli of the Klebsiella pneumoniae genes for production, surface localization and secretion of the lipoprotein pullulanase. EMBO J 6:3531–3538

    Google Scholar 

  • Day DF, Yaphe W (1975) Enzymatic hydrolysis of agar: purification and characterization of neoagarobiose hydrolase and p-nitrophenyl alpha-galactoside hydrolase. Can J Microbiol 21:1512–1518

    Article  CAS  Google Scholar 

  • Dong J, Hashikawa S, Konishi T, Tamaru Y, Araki T (2006) Cloning of the novel gene encoding beta-agarase C from a marine bacterium, Vibrio sp. strain PO-303, and characterization of the gene product. Appl Environ Microbiol 72:6399–6401

    Article  CAS  Google Scholar 

  • Dong J, Tamaru Y, Araki T (2007a) A unique beta-agarase, AgaA, from a marine bacterium, Vibrio sp. strain PO-303. Appl Microbiol Biotechnol 74:1248–1255

    Article  CAS  Google Scholar 

  • Dong J, Tamaru Y, Araki T (2007b) Molecular cloning, expression, and characterization of a beta-agarase gene, agaD, from a marine bacterium, Vibrio sp. strain PO-303. Biosci Biotechnol Biochem 71:38–46

    Article  CAS  Google Scholar 

  • Ekborg N, Gonzalez J, Howard M, Taylor E, Hutcheson S, Weiner R (2005) Saccharophagus degradans gen nov., sp. nov., a versatile marine degrader of complex polysaccharides. Int J Syst Evol Microbiol 55:1545–1549

    Article  CAS  Google Scholar 

  • Ekborg N, Taylor L, Weiner R, Hutcheson S (2006) Genomic and proteomic analysis of the agarolytic system of Saccharophagus degradans strain 2–40. Appl Environ Microbiol 72:3396–3405

    Article  CAS  Google Scholar 

  • Ensor L, Stotz SK, Weiner RM (1999) Expression of multiple insoluble complex polysaccharide degrading enzyme systems by a marine bacterium. J Ind Microbiol Biotechnol 23:123–126

    Article  CAS  Google Scholar 

  • Erikson D (1948) Differentiation of the vegetative and sporogenous phases of the actinomycetes. 3. Variation in the Actinomyces coelicolor species-group. J Gen Microbiol 2:252–259

    Google Scholar 

  • Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240

    Article  CAS  Google Scholar 

  • Flament D, Barbeyron T, Jam M, Potin P, Czjzek M, Kloareg B, Michel G (2007) Alpha-agarases define a new family of glycoside hydrolases, distinct from beta-agarase families. Appl Environ Microbiol 73:4691–4694

    Article  CAS  Google Scholar 

  • Fu W, Han B, Duan D, Liu W, Wang C (2008a) Purification and characterization of agarases from a marine bacterium Vibrio sp. F-6. J Ind Microbiol Biotechnol 35:915–922

    Article  CAS  Google Scholar 

  • Fu X, Kim S (2010) Agarases: review of major sources, categories, purification method, enzyme characteristics and application. Mar Drugs 8:200–218

    Article  CAS  Google Scholar 

  • Fu XT, Lin H, Kim SM (2008b) Purification and characterization of a novel beta-agarase, AgaA34, from Agarivorans albus YKW-34. Appl Microbiol Biotechnol 78:265–273

    Article  CAS  Google Scholar 

  • Fu XT, Pan CH, Lin H, Kim SM (2009) Gene cloning, expression, and characterization of a β-agarase, AgaB34, from Agarivorans albusYKW-34. J Microbiol Biotechnol 19:257–264

    Article  CAS  Google Scholar 

  • Giordano A, Andreotti G, Tramice A, Trincone A (2006) Marine glycosyl hydrolases in the hydrolysis and synthesis of oligosaccharides. Biotechnol J 1:511–530

    Article  CAS  Google Scholar 

  • Gonzalez J, Weiner R (2000) Phylogenetic characterization of marine bacterium strain 2–40, a degrader of complex polysaccharides. Int J Syst Evol Microbiol 50:831–834

    Article  Google Scholar 

  • Groleau D, Yaphe W (1977) Enzymatic hydrolysis of agar: purification and characterization of beta-neoagarotetraose hydrolase from Pseudomonas atlantica. Can J Microbiol 23:672–679

    Article  CAS  Google Scholar 

  • Ha SC, Lee S, Lee J, Kim HT, Ko HJ, Kim KH, Choi IG (2011) Crystal structure of a key enzyme in the agarolytic pathway, α-neoagarobiose hydrolase from Saccharophagus degradans 2–40. Biochem Biophys Res Commun 412:238–244

    Article  CAS  Google Scholar 

  • Hamer GK, Bhattacharjee SS, Yaphe W (1977) Analysis of the enzymic hydrolysis products of agarose by 13 C-n.m.r. spectroscopy. Carbohydr Res 54:7–l0

    Article  Google Scholar 

  • Hatada Y, Ohta Y, Horikoshi K (2006) Hyperproduction and application of alpha-agarase to enzymatic enhancement of antioxidant activity of porphyran. J Agric Food Chem 54:9895–9900

    Article  CAS  Google Scholar 

  • Hehemann JH, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G (2010a) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464:908–912

    Article  CAS  Google Scholar 

  • Hehemann JH, Michel G, Barbeyron T, Czjzek M (2010b) Expression, purification and preliminary X-ray diffraction analysis of the catalytic module of a beta-agarase from the flavobacterium Zobellia galactanivorans. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:413–417

    Article  Google Scholar 

  • Henrissat B, Davies G (1997) Structural and sequence-based classification of glycoside hydrolases. Curr Opin Struct Biol 7:637–644

    Article  CAS  Google Scholar 

  • Henshaw J, Horne-Bitschy A, van Bueren AL, Money VA, Bolam DN, Czjzek M, Ekborg NA, Weiner RM, Hutcheson SW, Davies GJ, Boraston AB, Gilbert HJ (2006) Family 6 carbohydrate binding modules in beta-agarases display exquisite selectivity for the nonreducing termini of agarose chains. J Biol Chem 281:17099–17107

    Article  CAS  Google Scholar 

  • Hopwood DA (1957) Genetic recombination in Streptomyces coelicolor. J Gen Microbiol 16:ii–iii

    Google Scholar 

  • Hutcheson SW, Zhang H, Suvorov M (2011) Carbohydrase systems of Saccharophagus degradans degrading marine complex polysaccharides. Mar Drugs 9:645–665

    Article  CAS  Google Scholar 

  • Jam M, Flament D, Allouch J, Potin P, Thion L, Kloareg B, Czjzek M, Helbert W, Michel G, Barbeyron T (2005) The endo-beta-agarases AgaA and AgaB from the marine bacterium Zobellia galactanivorans: two paralogue enzymes with different molecular organizations and catalytic behaviours. Biochem J 385703–385713

  • Ji MH (ed) (1997) Agar: seaweed chemistry. Science Press, Beijing, pp 5–26

    Google Scholar 

  • Kim H, Lee S, Lee D, Kim HS, Bang WG, Kim K, Choi IG (2010) Overexpression and molecular characterization of Aga50D from Saccharophagus degradans 2–40: an exo-type β-agarase producing neoagarobiose. Appl Microbiol Biotechnol 86:227–234

    Article  CAS  Google Scholar 

  • Kirimura K, Masuda N, Iwasaki Y, Nakagawa H, Kobayashi R, Usami S (1999) Purification and characterization of a novel beta-agarase from an alkalophilic bacterium, Alteromonas sp. E-1. J Biosci Bioeng 87:436–441

    Article  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 

  • Kobayashi R, Takisada M, Suzuki T, Kirimura K, Usami S (1997) Neoagarobiose as a novel moisturizer with whitening effect. Biosci Biotechnol Biochem 61:162–163

    Article  CAS  Google Scholar 

  • Lahaye M, Yaphe W, Viet MTP, Rochas C (1989) 13 C NMR spectroscopic investigation of methylated and charged agarose oligosaccharides and polysaccharides. Carbohydrate Res 190:249–265

    Article  CAS  Google Scholar 

  • Lee DG, Jang MK, Lee OH, Kim NY, Ju SA, Lee SH (2008) Overproduction of a glycoside hydrolase family 50 β-agarase from Agarivorans sp. JA-1 in Bacillus subtilis and the whitening effect of its product. Biotechnol Lett 30:911–918

    Article  CAS  Google Scholar 

  • Lee DG, Park GT, Kim NY, Lee EJ, Jang MK, Shin YG, Park GS, Kim TM, Lee JH, Lee JH, Kim SJ, Lee SH (2006) Cloning, expression, and characterization of a glycoside hydrolase family 50 beta-agarase from a marine Agarivorans isolate. Biotechnol Lett 28:1925–1932

    Article  CAS  Google Scholar 

  • Lee S, Lee J, Ha S, Shin D, Kim K, Choi IG (2009) Crystallization and preliminary X-ray analysis of neoagarobiose hydrolase from Saccharophagus degradans. Acta Crystallogr Sect F Struct Biol Cryst Commun 65:1299–1301

    Article  Google Scholar 

  • Liao L, Xu XW, Jiang XW, Cao Y, Yi N, Huo YY, Wu YH, Zhu XF, Zhang XQ, Wu M (2011) Cloning, expression, and characterization of a new beta-agarase from Vibrio sp. strain CN41. Appl Environ Microbiol 77:7077–7079

    Article  CAS  Google Scholar 

  • Lindén T, Peetre J, Hahn-Hägerdal B (1992) Isolation and characterization of acetic acid-tolerant galactose-fermenting strains of Saccharomyces cerevisiae from a spent sulfite liquor fermentation plant. Appl Environ Microbiol 58:1661–1669

    Google Scholar 

  • Long M, Yu Z, Xu X (2010) A novel β-agarase with high pH stability from marine Agarivorans sp. LQ48. Mar Biotechnol 12:62–69

    Article  CAS  Google Scholar 

  • Lu X, Chu Y, Wu Q, Gu Y, Han F, Yu W (2009) Cloning, expression and characterization of a new agarase-encoding gene from marine Pseudoalteromonas sp. Biotechnol Lett 31:1565–1570

    Article  CAS  Google Scholar 

  • Ma C, Lu X, Shi C, Li J, Gu Y, Ma Y, Chu Y, Han F, Gong Q, Yu W (2007) Molecular cloning and characterization of a novel beta-agarase, AgaB, from marine Pseudoalteromonas sp. CY24. J Biol Chem 282:3747–3754

    Article  CAS  Google Scholar 

  • McCandless E (1981) Polysaccharides of the seaweeds. In: Lobban C, Wynne M (eds) The biology of seaweeds. University of California Press, Berkeley, pp 559–588

    Google Scholar 

  • Michel G, Barbeyron T, Kloareg B, Czjzek M (2009) The family 6 carbohydrate-binding modules have coevolved with their appended catalytic modules toward similar substrate specificity. Glycobiology 19:615–623

    Article  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 71:23–33

    Article  CAS  Google Scholar 

  • Morrice LM, McLean MW, Long WF, Williamson FB (1983) β-Agarases I and II from Pseudomonas atlantica. Substrate specificities. Eur J Biochem 137:149–154

    Article  CAS  Google Scholar 

  • Ng-Ying-Kin NM, Yaphe W (1972) Properties of agar: parameters affecting gel-formation and the agarose-iodine reaction. Carbohydr Res 25:379–385

    Article  CAS  Google Scholar 

  • Oh C, Nikapitiya C, Lee Y, Whang I, Kim SJ, Kang DH, Lee J (2010) Cloning, purification and biochemical characterization of beta agarase from the marine bacterium Pseudoalteromonas sp. AG4. J Ind Microbiol Biotechnol 37:483–494

    Article  CAS  Google Scholar 

  • Ohta Y, Hatada Y, Ito S, Horikoshi K (2005a) High-level expression of a neoagarobiose-producing β-agarase gene from Agarivorans sp. JAMB-AII in Bacillus subtilis and enzymic properties of the recombinant enzyme. Biotechnol Appl Biochem 41:183–191

    Article  CAS  Google Scholar 

  • Ohta Y, Hatada Y, Miyazaki M, Nogi Y, Ito S, Horikoshi K (2005b) Purification and characterization of a novel α-agarase from a Thalassomonas sp. Curr Microbiol 50:212–216

    Article  CAS  Google Scholar 

  • Ohta Y, Hatada Y, Nogi Y, Li Z, Ito S, Horikoshi K (2004a) Cloning, expression, and characterization of a glycoside hydrolase family 86 beta-agarase from a deep-sea Microbulbifer-like isolate. Appl Microbiol Biotechnol 66:266–275

    Article  CAS  Google Scholar 

  • Ohta Y, Hatada Y, Nogi Y, Miyazaki M, Li Z, Akita M, Hidaka Y, Goda S, Ito S, Horikoshi K (2004b) Enzymatic properties and nucleotide and amino acid sequences of a thermostable beta-agarase from a novel species of deep-sea Microbulbifer. Appl Microbiol Biotechnol 64:505–514

    Article  CAS  Google Scholar 

  • Ohta Y, Nogi Y, Miyazaki M, Li Z, Hatada Y, Ito S, Horikoshi K (2004c) Enzymatic properties and nucleotide and amino acid sequences of a thermostable beta-agarase from the novel marine isolate, JAMBA94. Biosci Biotechnol Biochem 68:1073–1081

    Article  CAS  Google Scholar 

  • Potin P, Richard C, Rochas C, Kloareg B (1993) Purification and characterization of the alpha-agarase from Alteromonas agarlyticus (Cataldi) comb. nov., strain GJ1B. Eur J Biochem 214:599–607

    Article  CAS  Google Scholar 

  • Pugsley AP (1993) The complete general secretory pathway in gram negative bacteria. Microbiol Rev 57:50–108

    CAS  Google Scholar 

  • Pugsley AP, Chapon C, Schwartz M (1986) Extracellular pullulanase of Klebsiella pneumoniae is a lipoprotein. J Bacteriol 166:1083–1088

    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 iota-carrageenases. Biochemistry 49:7590–7599

    Article  CAS  Google Scholar 

  • Rebuffet E, Groisillier A, Thompson A, Jeudy A, Barbeyron T, Czjzek M, Michel G (2011) Discovery and structural characterization of a novel glycosidase family of marine origin. Environ Microbiol 13:1253–1270

    Article  CAS  Google Scholar 

  • Ren A, Xia ZX, Yu W, Zhou J (2010) Expression, crystallization and preliminary X-ray analysis of an anomeric inverting agarase from Pseudoalteromonas sp. CY24. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:1635–1639

    Article  Google Scholar 

  • Rhimi M, Chouayekh H, Gouillouard I, Maguin E, Bejar S (2011) Production of D-tagatose, a low caloric sweetener during milk fermentation using L-arabinose isomerase. Bioresour Technol 102:3309–3315

    Article  CAS  Google Scholar 

  • Rochas C, Potin P, Kloareg B (1994) NMR spectroscopic investigation of agarose oligomers produced by an alpha-agarase. Carbohydr Res 253:69–77

    Article  CAS  Google Scholar 

  • Seydel A, Gounon P, Pugsley AP (1999) Testing the “+2 rule” for lipoprotein sorting in the Escherichia coli cell envelope with a new genetic selection. Mol Microbiol 34:810–821

    Article  CAS  Google Scholar 

  • Shin M, Lee D, Skogerson K, Wohlgenuth G, Choi IG, Fiehn O, Kim K (2009) Global metabolic profiling of plant cell wall polysaccharide degradation by Saccharophagus degradans. Biotechnol Bioeng 105:477–488

    Article  Google Scholar 

  • Shin M, Lee D, Wohlgemuth G, Choi IG, Fiehn O, Kim K (2010) Global metabolite profiling of agarose degradation by Saccharophagus degradans 2–40. N Biotechnol 27:156–168

    Article  CAS  Google Scholar 

  • Smith SV (1981) Marine macrophytes as a global carbon sink. Science 211:838–840

    Article  CAS  Google Scholar 

  • Stanier RY (1942) Agar-decomposing strains of the Actinomyces coelicolor species-group. J Bacteriol 44:555–570

    CAS  Google Scholar 

  • Sugano Y, Kodama H, Terada I, Yamazaki Y, Noma M (1994) Purification and characterization of a novel enzyme, alpha-neoagarooligosaccharide hydrolase (alpha-NAOS hydrolase), from a marine bacterium, Vibrio sp. strain JT0107. J Bacteriol 176:6812–6818

    CAS  Google Scholar 

  • Sugano Y, Matsumoto T, Kodama H, Noma M (1993) Cloning and sequencing of agaA, a unique agarose 0107 gene from a marine bacterium, Vibrio sp. strain JT0107. Appl Environ Microbiol 59:3750–3756

    CAS  Google Scholar 

  • Suvorov M, Kumar R, Zhang H, Hutcheson S (2011) Novelties of the cellulolytic system of a marine bacterium applicable to cellulosic sugar production. Biofuels 2:59–70

    Article  CAS  Google Scholar 

  • Suzuki H, Sawai Y, Suzuki T, Kawai K (2002) Purification and characterization of an extracellular alpha-neoagarooligosaccharide hydrolase from Bacillus sp. MK03. J Biosci Bioeng 93:456–463

    CAS  Google Scholar 

  • Temuujin U, Chi WJ, Chang YK, Hong SK (2012) Identification and biochemical characterization of Sco3487 from Streptomyces coelicolor A3(2), an exo- and endo-type β-agarase-producing neoagarobiose. J Bacteriol 194:142–149

    Article  Google Scholar 

  • Temuujin U, Chi WJ, Lee SY, Chang YK, Hong SK (2011) Overexpression and biochemical characterization of DagA from Streptomyces coelicolor A3(2): an endo-type β-agarase producing neoagarotetraose and neoagarohexaose. Appl Microbiol Biotechnol 92:749–759

    Article  CAS  Google Scholar 

  • Usov AI (1998) Structural analysis of red seaweed galactans of agar and carrageenan groups. Food Hydrocolloids 12:301–308

    Article  CAS  Google Scholar 

  • van der Meulen HJ, Harder W (1976) Characterization of the neoagarotetra-ase and neoagarobi-ase of Cytophaga flevensis. Antonie van Leeuwenhoek 42:81–94

    Article  Google Scholar 

  • van de Velde F, Knutsen SH, Usov AI, Rollema HS, Cerezo AS (2002) 1H and 13C high resolution NMR spectroscopy of carrageenans: Application in research and industry. Trends Food Sci Technol 13:73–92

    Google Scholar 

  • Vockenhuber MP, Suess B (2011) Streptomyces coelicolor RNA scr5239 inhibits agarase expression by direct base pairing to dagA coding region. Microbiology. doi:10.1099/mic.0.54205-0

  • Wang J, Jiang X, Mou H, Guan H (2004) Anti-oxidation of agar oligosaccharides produced by agarase from a marine bacterium. J Appl Phycol 16:333–340

    Article  CAS  Google Scholar 

  • Wang J, Mou H, Jiang X, Guan H (2006a) Characterization of a novel β-agarase from marine Alteromonas sp. SY37-12 and its degrading products. Appl Microbiol Biotechnol 71:833–839

    Article  CAS  Google Scholar 

  • Wang Q, Wu C, Chen T, Chen X, Zhao X (2006b) Expression of galactose permease and pyruvate carboxylase in Escherichia coli ptsG mutant increases the growth rate and succinate yield under anaerobic conditions. Biotechnol Lett 28:89–93

    Article  Google Scholar 

  • Weiner R, Taylor L, Henrissat B, Hauser L, Land M, Coutinho P, Rancurel C, Saunders E, Longmire A, Zhang H, Bayer EA, Gilbert HJ, Larimer F, Zhulin IB, Ekborg NA, Lamed R, Richardson PM, Borovok I, Hutcheson S (2008) Complete genome sequence of the complex carbohydrate-degrading marine bacterium, Saccharophagus degradans strain 2–40. PLoS Genet 4:13

    Article  Google Scholar 

  • Whitehead LA, Stosz SK, Weiner RM (2001) Characterization of the agarase system of a multiple carbohydrate degrading marine bacterium. Cytobios 106:99–117

    CAS  Google Scholar 

  • Wu SC, Wen TN, Pan CL (2005) Algal-oligosaccharide-lysates prepared by two bacterial agarases stepwise hydrolyzed and their anti-oxidative properties. Fish Sci 71:1149–1159

    Article  CAS  Google Scholar 

  • Yanase H, Fukushi H, Ueda N, Maeda Y, Toyoda A, Tonomura K (1991) Cloning, sequencing, and characterization of the intracellular invertase gene from Zymomonas mobilis. Agric Biol Chem 55:1383–1390

    Article  CAS  Google Scholar 

  • Yang JI, Chen LC, Shih YY, Hsieh C, Chen CY, Chen WM, Chen CC (2011) Cloning and characterization of β-agarase AgaYT from Flammeovirga yaeyamensis strain YT. J Biosci Bioeng 112:225–232

    Article  CAS  Google Scholar 

  • Yun E, Shin M, Yoon JJ, Kim Y, Choi IG, Kim K (2011) Production of 3,6-anhydro-L-galactose from agarose by agarolytic enzymes of Saccharophagus degradans 2–40. Process Biochem 46:88–93

    Article  CAS  Google Scholar 

  • Zhang W, Sun L (2007) Cloning, characterization and molecular application of a beta-agarase gene from Vibrio sp. strain V134. Appl Environ Microbiol 73:2825–2831

    Article  CAS  Google Scholar 

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Acknowledgment

This work was supported by grant no. SA00004146 from the Next-Generation BioGreen 21 Program, Rural Development Administration, Republic of Korea.

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  1. Division of Bioscience and Bioinformatics, Myongji University, Yongin, Gyeonggi-do, 449-728, Korea

    Won-Jae Chi & Soon-Kwang Hong

  2. Department of Chemical and Biomolecular Engineering, Korea Advanced Institute of Science and Technology, 373-1, Kusong-dong, Yusung-gu, Taejon, 305-701, Korea

    Yong-Keun Chang

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  1. Won-Jae Chi
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Chi, WJ., Chang, YK. & Hong, SK. Agar degradation by microorganisms and agar-degrading enzymes. Appl Microbiol Biotechnol 94, 917–930 (2012). https://doi.org/10.1007/s00253-012-4023-2

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Keywords

  • Agar
  • Agarose
  • Porphyran
  • Agarase
  • Porphyranase
  • Agar degradation