Revisiting the Cellulosimicrobium cellulans yeast-lytic β-1,3-glucanases toolbox: A review
© Ferrer; licensee BioMed Central Ltd. 2006
Received: 14 November 2005
Accepted: 17 March 2006
Published: 17 March 2006
Cellulosimicrobium cellulans (also known with the synonyms Cellulomonas cellulans, Oerskovia xanthineolytica, and Arthrobacter luteus) is an actinomycete that excretes yeast cell wall lytic enzyme complexes containing endo-β-1,3-glucanases [EC 184.108.40.206 and 220.127.116.11] as key constituents. Three genes encoding endo-β-1,3-glucanases from two C. cellulans strains have been cloned and characterised over the past years. The βglII and βglII A genes from strain DSM 10297 (also known as O. xanthineolytica LL G109) encoded proteins of 40.8 and 28.6 kDa, respectively, whereas the β-1,3-glucanase gene from strain ATCC 21606 (also known as A. luteus 73–14) encoded a 54.5 kDa protein. Alignment of their deduced amino acid sequences reveal that βglII and βglII A have catalytic domains assigned to family 16 of glycosyl hydrolases, whereas the catalytic domain from the 54.5 kDa glucanase belongs to family 64. Notably, both βglII and the 54.5 kDa β-1,3-glucanase are multidomain proteins, having a lectin-like C-terminal domain that has been assigned to family 13 of carbohydrate binding modules, and that confers to β-1,3-glucanases the ability to lyse viable yeast cells. Furthermore, βglII may also undergo posttranslational proteolytic processing of its C-terminal domain, resulting in a truncated enzyme retaining its glucanase activity but with very low yeast-lytic activity. In this review, the diversity in terms of structural and functional characteristics of the C. cellulans β-1,3-glucanases has been compiled and compared.
Several bacteria have been reported to be able to lyse and grow on viable yeast and fungal cells by producing a variety of cell-wall degrading enzymes such as endo-β-1,3-glucanases, proteases, β-1,6-glucanases, mannanases, and chitinases. The structural complexity of the yeast cell wall, which is mainly composed of complex polymers of β-1,3- and β-1,6-glucans, mannoproteins, and smaller amounts of chitin [1, 2], implies that the synergistic action of these enzymes is necessary to hydrolyse its components into assimilable substrates. Nevertheless, endo-β-1,3-glucanases [EC 18.104.22.168 and EC 22.214.171.124] have been considered to play a major role in yeast cell lysis [2, 3].
The actinomycete Cellulosimicrobium cellulans (also known with the synonyms Cellulomonas cellulans, Oerskovia xanthineolytica, and Arthrobacter luteus), has been regarded as a major source of yeast-lytic enzymes, particularly endo-β-1,3-glucanases, proteases and mannanases. Notably, several commercially available yeast-lytic glucanases preparations derived from this organism, namely Lyticase, Zymolyase, and Quantazyme, have been widely used for yeast protoplast preparation and yeast DNA isolation. Endo-β-1,3-glucanases are the major component of such enzyme preparations. Only one of these commercially available preparations (Quantazyme, Quantum Biotechnology, Canada) is produced recombinantly and protease-free. Besides their application in spheroplasting, C. cellulans β-1,3-glucanases have shown their big potential in a wide range of applications in both basic research and biotechnology; for instance, in structural analyses of the yeast and fungal cell wall [4, 5], in cell wall permeabilisation for the selective recombinant protein recovery from yeast cells [6, 7], or in biocatalysis [8–10], among others.
Early characterisation studies on the lytic enzyme system from different C. cellulans strains showed that this organism excreted a wide heterogeneity of β-1,3-glucanase forms with different physicochemical and functional properties [11–15]. Notably, while all of the isolated forms showed hydrolytic activity toward β-glucans (glucanase activity), only some were found capable of inducing lysis of viable yeast cells (lytic activity).
The cloning and sequencing of three β-1,3-glucanase-encoding genes from C. cellulans has allowed for further molecular and biochemical characterisation studies over the past years. These studies have revealed the diversity in terms of structural and functional characteristics of the C. cellulans β-1,3-glucanases, which have been compiled and compared in this review.
Origin of the multiplicity of β-1,3-glucanases isoforms
Summary of β-1,3-glucanases from Cellulosimicrobium cellulans
Catalytic domain GH family
Km (mg ml- 1) c
pH optimum c
Lytic activity b
Strain DSM 10297 Native βglIIt
Native β-1,3- glucanase
Strain ATCC 21606
Native β-1,3- glucanase
In contrast, only one gene could be isolated from a C. cellulans ATCC 21606 genomic library . Nevertheless, southern blot hybridization studies suggest that strain ATCC 21606 also has a βglII-like gene .
Functional properties of C. cellulans β-1,3-glucanases
As discussed below, while the β-1,3-glucanase isolated from strain ATCC 21606 has been classified in family 64 of glycosyl hydrolases (GH-64), β-1,3-glucanases from strain DSM 10297 have been classified in family 16 of glycosyl hydrolases (GH-16), thus revealing an important structural diversity [24, 25]. This is further reflected in the heterogeneity of C. cellulans functional characteristics:
Although all C. cellulans β-1,3-glucanases hydrolyse yeast glucan in an endolytic manner, GH-16 β-1,3-glucanases yield a mixture of biose and glucose , whereas GH-64 β-1,3-glucanases hydrolyse yeast glucan with predominant liberation of pentoses .
Enzymatic hydrolysis of glycosidic bonds occurs with two possible stereochemical outcomes: inversion or retention of the anomeric configuration at the site of cleavage. 'Inverting' enzymes utilise a single-displacement reaction where an activated water molecule performs a nucleophilic attack at the sugar C-1 while concomitant aglycone departure is achieved by protonation of the glycosilic oxygen. By contrast, 'retaining' enzymes utilise a double-displacement mechanism involving a covalent glycosyl-enzyme intermediate.
The stereochemistry of hydrolysis in family GH-64 β-1,3-glucanases has been recently determined for one of its members, a β-1,3-glucanase from Streptomyces matensis . Interestingly, while family GH-16 β-glucanases have been shown to be 'retaining' enzymes , this GH-64 enzyme is the first inverting β-1,3-glucanase characterised. The inverting mechanism implies that the molecular mechanism of hydrolysis by this enzyme does not involve the formation of a covalent glycosyl-enzyme intermediate. Since the molecular mechanism has been shown to be conserved within the families of glycoside hydrolases, it can be concluded that family GH-64 glycoside hydrolases may operate by an inverting mechanism .
The differences in "yeast-lytic" activity of the different β-1,3-glucanases forms is reflected in their kinetic properties (table 1). For instance, the 27.2 kDa βglIIt form (i.e. with no carbohydrate binding module) has very low yeast lytic activity; correspondingly, its K m for yeast glucan (insoluble) is higher than for the soluble substrate (laminarin). In contrast, a β-1,3-glucanase with high lytic activity such as the one from ATCC 21606 strain (having a C-terminal carbohydrate-binding domain, as discussed below), has a K m for yeast glucan lower than for laminarin . Another interesting observation concerns the possible effect of a carbohydrate-binding domain in the catalytic properties for soluble substrates of the catalytic domain is attached to. In particular, the presence of a carbohydrate-binding domain in the recombinant βglII seems to increase the K m for laminarin in relation to the native βglIIt form (table 1), .
β-1,3-glucanase forms isolated from C. cellulans appear to have a pH optimum in the range of 5.5 to 8 (depending on the substrate), with the exception of the βglII A enzyme from strain DSM 10297, which seems to have an acidic pH of about 4.0 . It is also remarkable that the GH-16 β-1,3-glucanases from C. cellulans so far characterised (βglII from strain DSM 10297 and the β-1,3-glucanase from the strain known as O. xanthineolytica TK-1 ) have a moderately high optimum activity temperature (table 1). However, only the native βglIIt enzyme has been shown to have a significant thermotolerance (the enzyme retained about 50% of its residual activity after 30' of incubation at 70°C, pH 7 ).
Sequence analysis of C. cellulans β-1,3-glucanases
In contrast, the 380 aa catalytic domain of the yeast-lytic 54.5 kDa β-1,3-glucanase from C. cellulans ATCC 21606 , has been classified into GH-64 family. Interestingly, this β-1,3-glucanase is a modular enzyme, having a C-terminal "lytic domain" of about 120 aa that falls into the CBM family 13 (figure 1).
βglII shows the highest similarity values, ranging from about 60 % to 40 % of sequence identity in 240 aa overlaps, to the GH-16 bacterial endo-1,3-β-glucanases (laminarinases) subfamily members, as well as to several non-bacterial β-1,3-glucan-acting proteins such as the β-1,3-glucanase LamA from the archeon Pyrococcus furiosus (GenBank accession number AF013169) , 49 % identity, the β-1,3-glucanase from Strongylocentrotus purpuratus (sea urchin), (GenBank accession number U49711) , 36.6% identity, and to the α-subunit of the (1→3)β-D-glucan-sensitive coagulation factor G from Tachypleus tridentatus (horseshoe crab), (GenBank accession number D16622) , 39.5% identity. Sequence identity values between βglII and the GH-16 bacterial 1,3-1,4-β-glucan 4-glucanohydrolases (lichenases) subfamily members are somewhat lower (ca. 25%). Detailed similarity and phylogenetic analyses have been reported for GH-16 enzymes [28, 37]. Secondary structure analyses of the native 27.2 kDa βglIIt form revealed a high content of β-structure and the presence of a compact hydrophobic core including the presence of several tryptophan residues , which is consistent with the characteristic jellyroll β-sandwich fold of bacterial family 16 β-glucanases .
The sequence WPSSGEIDIME, which includes de catalytic glutamate residues of the active site conserved within GH-16 , was identified between residues 166 to 176 and 177 to 187 of the βglII and βglII A precursors, respectively. Also, the Met residue of this motif, which is invariant in GH-16 laminarinases subfamily but not present in the active site of the GH-16 lichenases subfamily members, is likely to have an important structural role in the active site of βglII, as observed in the Rhodothermus marinus LamR laminarinase and bglA β-glucanase [39, 39] and the archeon Pyrococcus furiosus LamA laminarisase ). Notably, the βglIIt form purified from strain DSM 10297 has been shown to be able to hydrolyse both β-1,3- and β-1,3-1- 4-glucan (lichenan) , as reported for some other members of the GH-16 laminarinases subfamily [39, 39]. As noted earlier , it is remarkable that GH-16 β-1,3-glucanases have 9 highly conserved tryptophan residues.
Sequence identity of the 54.5 kDa β-1,3-glucanase from C. cellulans ATCC 21606 GH-64 catalytic domain with other β-1,3-glucanases of this family of glycosyl hydrolases ranges from 99% identity to the β-1,3-glucanase of Arthrobacter sp. YCWD3 (GenBank accession number D23668) to 60% and 31% to the Laminaripentaose-Producing β-1,3-glucanase of Streptomyces matensis DIC-108  and the β-1,3-glucanase B from Lysobacter enzymogenes , respectively. In contrast to β-1,3-glucanases from strain ATCC 21606 and Arthrobacter sp. YCWD3, the β-1,3-glucanases from S. matensis and L. enzymogenes do not contain the carbohydrate-binding modules at the C-terminus. This indicates that the liberation of only laminaripentaose as the degradation product from β-1,3-glucan observed for this family of enzymes is not related to their CBM. The 54.5 kDa β-1,3-glucanase GH-64 catalytic domain from strain ATCC 21606 shares a very low sequence identity to βglII and βglII A GH-16 catalytic domains (15% and 19%, respectively, over the entire domain). Similarity and phylogenetic analyses have also been reported for GH-64 enzymes .
Truncated yeast/fungi-lytic β-glucanases, chitinases and proteases lacking their corresponding CBMs show reduced activities against viable yeast/fungal cells while retaining their capacity to depolymerise colloidal glucan or chitin, or to degrade proteins [16, 41, 46, 46]. As summarised above, the proteolytic removal of the CBM from βglII dramatically reduces its capability to lyse viable yeast cells. However, the ability of the βglIIt form to lyse viable yeast cell walls is restored in the presence of the yeast-lytic protease component secreted by C. cellulans . This synergistic effect between the βglIIt form and the lytic proteases suggests that the affinity of this β-1,3-glucanase for the glucan layer of the cell wall does not depend on the possession of the carbohydrate-binding domain, as it can readily solubilise the glucan component of the yeast cell wall when the outer mannoprotein layer is removed by the proteases. However, there is no reported evidence on whether the CBM may have any effect on the K m values of βglII for insoluble substrates such as yeast glucan. Affinity of the βglII catalytic domain to polysaccharides could be partially conferred by some of the highly conserved tryptophan residues, as observed in some polysaccharide-binding proteins . Interestingly, some of these residues are believed to be located at the surface of the GH-16 LamR laminarinase from R. marinus .
Considering that the ricin B-chain exhibits galactose-binding activity and has a specifically high affinity for the oligosaccharides from cell wall surfaces (it binds much more strongly to complex galactosides from cell wall surface carbohydrates than to simple sugars, ), its similarity to the βglII C-terminal repeats suggests that these constitute a lectin-like domain with binding activity towards oligosaccharides of the yeast cell wall surface, which are rich in mannose. In addition, the similarity of this domain with the R. faecitabidus yeast-lytic Protease I mannose-binding domain and the strain ATCC 21606 β-1,3-glucanase carbohydrate-binding domains, leads to the conclusion that the C-terminal domain of these C. cellulans β-1,3-glucanases is a mannose-binding module, and that it is also essential for efficient lytic activity towards viable yeast cells. Mannose-binding domains may play an important general function in targeting yeast/fungi-lytic enzymes to their substrates by increasing their local concentration on the yeast/fungal cell wall surface, which is rich in mannoproteins. Recent studies on the S. cerevisiae cell wall architecture using Quantazyme ylg (i.e. the pure recombinant β-1,3-glucanase preparation from C. cellulans ATCC 21606) have revealed that this enzyme is able to release cell wall mannoproteins by cleaving β-1,3-chains, to which these cell wall proteins are attached . However, the mode of action of βglII and its precise target on its natural substrate, the yeast cell wall, is still unknown. It is significant that C. cellulans can co-produce modular and non-modular β-1,3-glucanases, either by proteolytic digestion of modular species, or by expressing specific genes, suggesting that these truncated versions have also an important role in cell wall degradation (figure 1). At this stage, it is apparent that more comprehensive studies are needed in order to evaluate the specific role of modular and non-modular yeast/fungi lytic β-1,3-glucanases on the yeast cell wall degradation, and their interactions with other lytic enzymes secreted by these bacteria.
Besides C. cellulans, there are other prokaryotes, such as L. enzymogenes and S. coelicolor, known to produce multiple β-1,3-glucanase systems with the ability to lyse fungal/yeast cells. These three species contain both GH-64 and GH-16 enzymes. Furthermore, these β-1,3-glucanase systems share significant similarities in terms of structural organisation. For instance, GluC and GluA from L. enzymogenes, and βglII and βglII A from C. cellulans have GH-16 catalytic domains;gluC and βglII contain a substrate-binding domain located at their C-terminal that is lacking in GluA and βglII A . Interestingly, the substrate-binding C-terminal regions observed in some of these β-1,3-glucanases belong to different CBM families, namely family 13 for C. cellulans glucanases and, family 6 for L. enzymogenes . This diversity observed among enzyme type and source organism is a trait indicative of domain shuffling in the evolution of glycosyl hydrolases.
Availability of recombinant C. cellulans β-1,3-glucanases has opened the door to comprehensive characterisation (and future engineering) of these biotechnologically important enzymes, which is key for the development of new/potential applications or the optimisation the existing ones. Nevertheless, a better understanding of the basis of the substrate specificity and interactions with the yeast cell wall components still awaits a detailed comparison of the three-dimensional structures of these enzymes and systematic experimental verifications of the derived conclusions by protein engineering.
- Klis FM: Review: cell wall assembly in yeast. Yeast. 1994, 10: 851-869. 10.1002/yea.320100702.View ArticleGoogle Scholar
- Fleet GH: Cell walls. The Yeasts. Edited by: Rose AH, Harrison JS. 1991, London, Academic Press, 4: 199-277.Google Scholar
- Bielecki S, Galas E: Microbial β-glucanases different form cellulases. Crit Rev Biotechnol. 1991, 10: 275-304.View ArticleGoogle Scholar
- Kollár R, Reinhold BB, Petáková E, Yeh HJC, Ashwell G, Drgonova J, Kapteyn JC, Klis FM, Cabib E: Architecture of the yeast cell wall. β (1→6)-glucan interconnects mannoprotein, β (1→3)glucan, and chitin. J Biol Chem. 1997, 272: 17762-17775. 10.1074/jbc.272.28.17762.View ArticleGoogle Scholar
- Kapteyn JC, Montijn RC, Vink E, de la Cruz J, Llobell A, Douwes JE, Shimoi H, Lipke P, Klis FM: Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked β-1,3-/β-1,6-glucan heteropolymer. Glycobiol. 1996, 6: 337-345.View ArticleGoogle Scholar
- Shen S-H, Bastien L, Nguyen T, Fung M, Slilaty SN: Synthesis and secretion of hepatitis B middle surface antigen by the methylotrophic yeast Hansenula polymorpha . Gene. 1989, 84: 303-309. 10.1016/0378-1119(89)90504-0.View ArticleGoogle Scholar
- Asenjo JA, Ventom AM, Huang R-B, Andrews BA: Selective release of recombinant protein particles (VLPs) from yeast using a pure lytic glucanase enzyme. Bio/Technology. 1993, 11: 214-217. 10.1038/nbt0293-214.View ArticleGoogle Scholar
- Borriss R, Krah M, Brumer H, Kerzhner MA, Ivanen DR, Eneyskaya EV, Elyakova LA, Shishlyannikov SM, Shabalin KA, Neustroev KN: Enzymatic synthesis of 4-methylumbelliferyl (1→3)-β-D-glucooligosaccharides – new substrates for β-1,3-1,4-D-glucanase. Carbohydr Res. 2003, 338: 1455-1467. 10.1016/S0008-6215(03)00199-X.View ArticleGoogle Scholar
- Buchowiecka A, Bielecki S: Specificity of endo-β-1,3-glucanase G A from Cellulomonas cellulans towards structurally diversified acceptor molecules in transglycosylation reaction. Biocatal Biotransform. 2002, 20: 95-100. 10.1080/10242420290018078.View ArticleGoogle Scholar
- Buchowiecka A, Bielecki S: Determination of the regioselectivity of D-glucal glucosylation by endo-β-1,3-glucanase G A from Cellulomonas cellulans using CI MS. Biocatal Biotransform. 2003, 21: 1-5. 10.1080/1024242031000076206.View ArticleGoogle Scholar
- Doi K, Doi A, Ozaki T, Fukui T: Further studies on the heterogeneity of the lytic activity for isolated yeast cell walls of the components of an Arthrobacter glucanase system: properties of the two components of a β-(1→3)-glucanase. Agric Biol Chem. 1976, 40: 1355-1362.View ArticleGoogle Scholar
- Vrsanská M, Biely P, Krátký Z: Enzymes of the yeast lytic system produced by Arthrobacter GJM-1 bacterium and their role in the lysis of yeast cell walls. Z Allg Mikrobiol. 1977, 17: 465-480.View ArticleGoogle Scholar
- Obata T, Fujioka S, Hara S, Namba Y: The synergistic effects among β-(1→3)-glucanases from Oerskovia sp CK on lysis of viable yeast cells. Agric Biol Chem. 1977, 41: 671-677.View ArticleGoogle Scholar
- Jeffries TW, Macmillan JD: Action patterns fo (1→3)-β-D-glucanases from Oerskovia xanthineolytica on laminarin, lichenan and yeast glucan. Carbohydr Res. 1981, 95: 87-100. 10.1016/S0008-6215(00)85298-2.View ArticleGoogle Scholar
- Scott JH, Schekman R: Lyticase: endoglucanase and protease activities that act together in yeast cell lysis. J Bacteriol. 1980, 142: 414-423.Google Scholar
- Shen SH, Chrétien P, Bastien L, Slilaty SN: Primary sequence of the glucanase gene from Oerskovia xanthineolytica . J Biol Chem. 1991, 266: 1058-1063.Google Scholar
- Ferrer P, Hedegaard T, Halkier T, Diers I, Savva D, Asenjo JA: Molecular cloning of a lytic β-1,3-glucanase gene from Oerskovia xanthineolytica LL G109. Ann NY Acad Sci. 1996, 782: 555-666.View ArticleGoogle Scholar
- Ferrer P, Halkier T, Hedegaard L, Savva D, Diers I, Asenjo JA: Nucleotide sequence of a β-1,3-glucanase isoenzyme II A gene of Oerskovia xanthineolytica LL G109 (Cellulomonas cellulans) and initial characterization of the recombinant enzyme. J Bacteriol. 1996, 178: 4751-4757.Google Scholar
- Ferrer P, Diers I, Halkier T, Hedegaard L: Patent WO97/39114. 1997Google Scholar
- Salazar O, Molitor J, Lienqueo ME, Asenjo JA: Overproduction, purification and characterization of β-1,3-glucanase type II in Escherichia coli. Prot Expres Purif. 2001, 23: 219-225. 10.1006/prep.2001.1497.View ArticleGoogle Scholar
- Parrado J, Escuredo PR, Conejero-Lara F, Kotik M, Ponting CP, Asenjo JA, Dobson CM: Molecular characterisation of a thermoactive β-1,3-glucanase from Oerskovia xanthineolytica . Biochim Biophys Acta. 1996, 1296: 145-151.View ArticleGoogle Scholar
- Ventom AM, Asenjo JA: Characterization of yeast lytic enzymes from Oerskovia xanthineolytica LL-G109. Enzyme Microb Technol. 1991, 13: 71-75. 10.1016/0141-0229(91)90191-C.View ArticleGoogle Scholar
- Ferrer P: PhD Thesis. 1995, The University of Reading, U.KGoogle Scholar
- Henrissat B, Bairoch A: New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 1993, 293: 781-788.View ArticleGoogle Scholar
- Coutinho PM, Henrissat B: Carbohydrate-active enzymes: an integrated database approach. Recent Advances in Carbohydrate Bioengineering. Edited by: Gilbert H, Davies G, Henrissat B, Svensson B. 1999, The Royal Society of Chemistry, Cambridge, 3-12.Google Scholar
- Saeki K, Iwata J, Yamazaki S, Watanabe Y, Tamai Y: Purification and characterization of a yeast lytic β-1,3-glucanase from Oerskovia xanthineolytica TK-1. J Ferment Bioeng. 1994, 78: 407-412. 10.1016/0922-338X(94)90038-8.View ArticleGoogle Scholar
- Nishimura T, Bignon C, Allouch J, Czjzek M, Darbon H, Watanabe T, Henrissat B: Streptomyces matensis laminaripentaose hydrolase is an 'inverting' β-1,3-glucanase. FEBS Lett. 2001, 499: 187-190. 10.1016/S0014-5793(01)02551-0.View ArticleGoogle Scholar
- Planas A: Bacterial 1,3-1,4-β-glucanases: structure, function and protein engineering. Biochim Biophys Acta. 2000, 1543: 361-382.View ArticleGoogle Scholar
- Altschul SF, Maddeen TL, Schäffer A, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res. 1997, 25: 3389-3402. 10.1093/nar/25.17.3389.View ArticleGoogle Scholar
- National Center for Biotechnology Information. [http://www.ncbi.nlm.nih.gov/]
- Coutinho PM, Henrissat B: Carbohydrate-Active Enzymes server at URL. 1999, [http://afmb.cnrs-mrs.fr/CAZY/]Google Scholar
- Tomme P, Warren RA, Gilkes NR: Cellulose hydrolysis by bacteria and fungi. Adv Microb Physiol. 1995, 37: 1-81.View ArticleGoogle Scholar
- Tomme P, Warren RA, Miller RC, Kilburn DG, Gilkes NR: Cellulose-binding domains: classification and properties. Enzymatic Degradation of Insoluble Polysaccharides. Edited by: Saddler JN, Penner M. 1995, American Chemical Society, Washington, 142-163.Google Scholar
- Guergen Y, Voorhorst WGB, van der Oost J, de Vos WM: Molecular and biochemical characterization of an endo-β-1,3-glucanase of the hyperthermophilic archaeon Pyrococcus furiosus . J Biol Chem. 1997, 272: 31258-31264. 10.1074/jbc.272.50.31258.View ArticleGoogle Scholar
- Bachman ES, McClay DR: Molecular cloning of the first metazoan beta-1,3 glucanase from eggs of the sea urchin Strongylocentrotus purpuratus. Proc Natl Acad Sci U.S.A. 1996, 93: 6808-6813. 10.1073/pnas.93.13.6808.View ArticleGoogle Scholar
- Seki N, Muta T, Oda T, Iwaki D, Kuma K, Miyata T, Iwanaga S: Horseshoe crab (1,3)-beta-D-glucan-sensitive coagulation factor G. A serine protease zymogen heterodimer with similarities to beta-glucan-binding proteins. J Biol Chem. 1994, 269: 1370-1374.Google Scholar
- Palumbo JD, Sullivan RF, Kobayashi DY: Molecular characterization and expression in Escherichia coli of three beta-1,3-glucanase genes from Lysobacter enzymogenes strain N4-7. J Bacteriol. 2003, 185: 4362-4370. 10.1128/JB.185.15.4362-4370.2003.View ArticleGoogle Scholar
- Krah M, Misselwitz R, Politz O, Thomsen KK, Welfle H, Borriss R: The laminarinase from thermophilic eubacterium Rhodothermus marinus – conformation, stability, and identification of active site carboxylic residues by site-directed mutagenesis. Eur J Biochem. 1998, 257: 101-111. 10.1046/j.1432-1327.1998.2570101.x.View ArticleGoogle Scholar
- Spilliaert R, Hreggvidsson GO, Kristjansson JK, Eggertsson G, Palsdottir A: Cloning and sequencing of a Rhodothermus marinus gene, bglA, coding for a thermostable beta-glucanase and its expression in Escherichia coli. Eur J Biochem. 1994, 224: 923-930. 10.1111/j.1432-1033.1994.00923.x.View ArticleGoogle Scholar
- Nakabayashi M, Nishijima T, Ehara G, Nikaidou N, Nishihashi H, Watanabe T: Structure of the gene encoding laminaripentaose-producing β-1,3-glucanase (LPHase) of Streptomyces matensis DIC-108. J Ferment Bioeng. 1998, 85: 459-464. 10.1016/S0922-338X(98)80062-7.View ArticleGoogle Scholar
- Shimoi H, Iimura Y, Obata T, Tadenuma M: Molecular structure of Rarobacter faecitabidus Protease I. A yeast-lytic serine protease having mannose-binding activity. J Biol Chem. 1992, 267: 25189-25195.Google Scholar
- Roberts LM, Lamb FI, Pappin DJ, Lord JM: The primary sequence of Ricinus communis agglutinin. Comparison with ricin. J Biol Chem. 1985, 260: 15682-15686.Google Scholar
- Tregear JW, Roberts LM: The lectin gene family of Ricinus communis : cloning of a functional ricin gene and three lectin pseudogenes. Plant Mol Biol. 1992, 18: 515-525. 10.1007/BF00040667.View ArticleGoogle Scholar
- Rutenber E, Robertus JD: Structure of ricin B-chain at 2.5 Å resolution. Proteins. 1991, 10: 260-269. 10.1002/prot.340100310.View ArticleGoogle Scholar
- Watanabe T, Ito Y, Yamada T, Hashimoto M, Sekine S, Tanaka H: The roles of the C-terminal domain and type III domains of chitinase A1 from Bacillus circulans WL-12 in chitin degradation. J Bacteriol. 1994, 176: 4465-4472.Google Scholar
- Watanabe T, Kasahara N, Aida K, Tanaka H: Three N-terminal domains fo β-1,3-glucanase A1 are involved in binding to insoluble β-1,3-glucan. J Bacteriol. 1992, 174: 186-190.Google Scholar
- Din N, Forsythe LJ, Burtnick LD, Gilkes NR, Miller RC, Warren RAJ, Kilburn DG: The cellulose-binding domain of endoglucanase A (CenA) from Cellulomonas fimi : evidence for the involvement of tryptophan residues in binding. Mol Microbiol. 1994, 11: 747-755.View ArticleGoogle Scholar
- Monfort W, Villafranca JE, Monzingo AF, Ernst SR, Katzin B, Rutenber E, Xuong N, Hamlin R, Robertus JD: The three-dimensional structure of ricin at 2.8 Å. J Biol Chem. 1987, 262: 5398-5403.Google Scholar
- Tsujibo H, Ohtsuki T, Iio T, Yamazaki I, Miyamoto K, Sugiyama M, Inamori Y: Cloning and sequence analysis of genes encoding xylanases and acetyl xylan esterase from Streptomyces thermoviolaceus OPC-520. Appl Environ Microbiol. 1997, 63: 661-664.Google Scholar
- Shareck F, Roy C, Yaguchi M, Morosoli R, Kluepfel D: Sequences of three genes specifying xylanases in Streptomyces lividans. Gene. 1991, 107: 75-82. 10.1016/0378-1119(91)90299-Q.View ArticleGoogle Scholar
- Vincent P, Shareck F, Dupont C, Morosoli R, Kluepfel D: New alpha-L-arabinofuranosidase produced by Streptomyces lividans : cloning and DNA sequence of the abfB gene and characterization of the enzyme. Biochem J. 1997, 322: 845-852.View ArticleGoogle Scholar
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