Functional diversity of three tandem C-terminal carbohydrate-binding modules of a β-mannanase
2021; Elsevier BV; Volume: 296; Linguagem: Inglês
10.1016/j.jbc.2021.100638
ISSN1083-351X
AutoresMarie Sofie Møller, Souad El Bouaballati, Bernard Henrissat, Birte Svensson,
Tópico(s)Polysaccharides and Plant Cell Walls
ResumoCarbohydrate active enzymes, such as those involved in plant cell wall and storage polysaccharide biosynthesis and deconstruction, often contain repeating noncatalytic carbohydrate-binding modules (CBMs) to compensate for low-affinity binding typical of protein–carbohydrate interactions. The bacterium Saccharophagus degradans produces an endo-β-mannanase of glycoside hydrolase family 5 subfamily 8 with three phylogenetically distinct family 10 CBMs located C-terminally from the catalytic domain (SdGH5_8-CBM10x3). However, the functional roles and cooperativity of these CBM domains in polysaccharide binding are not clear. To learn more, we studied the full-length enzyme, three stepwise CBM family 10 (CBM10) truncations, and GFP fusions of the individual CBM10s and all three domains together by pull-down assays, affinity gel electrophoresis, and activity assays. Only the C-terminal CBM10-3 was found to bind strongly to microcrystalline cellulose (dissociation constant, Kd = 1.48 μM). CBM10-3 and CBM10-2 bound galactomannan with similar affinity (Kd = 0.2–0.4 mg/ml), but CBM10-1 had 20-fold lower affinity for this substrate. CBM10 truncations barely affected specific activity on carob galactomannan and konjac glucomannan. Full-length SdGH5_8-CBM10x3 was twofold more active on the highly galactose-decorated viscous guar gum galactomannan and crystalline ivory nut mannan at high enzyme concentrations, but the specific activity was fourfold to ninefold reduced at low enzyme and substrate concentrations compared with the enzyme lacking CBM10-2 and CBM10-3. Comparison of activity and binding data for the different enzyme forms indicates unproductive and productive polysaccharide binding to occur. We conclude that the C-terminal-most CBM10-3 secures firm binding, with contribution from CBM10-2, which with CBM10-1 also provides spatial flexibility. Carbohydrate active enzymes, such as those involved in plant cell wall and storage polysaccharide biosynthesis and deconstruction, often contain repeating noncatalytic carbohydrate-binding modules (CBMs) to compensate for low-affinity binding typical of protein–carbohydrate interactions. The bacterium Saccharophagus degradans produces an endo-β-mannanase of glycoside hydrolase family 5 subfamily 8 with three phylogenetically distinct family 10 CBMs located C-terminally from the catalytic domain (SdGH5_8-CBM10x3). However, the functional roles and cooperativity of these CBM domains in polysaccharide binding are not clear. To learn more, we studied the full-length enzyme, three stepwise CBM family 10 (CBM10) truncations, and GFP fusions of the individual CBM10s and all three domains together by pull-down assays, affinity gel electrophoresis, and activity assays. Only the C-terminal CBM10-3 was found to bind strongly to microcrystalline cellulose (dissociation constant, Kd = 1.48 μM). CBM10-3 and CBM10-2 bound galactomannan with similar affinity (Kd = 0.2–0.4 mg/ml), but CBM10-1 had 20-fold lower affinity for this substrate. CBM10 truncations barely affected specific activity on carob galactomannan and konjac glucomannan. Full-length SdGH5_8-CBM10x3 was twofold more active on the highly galactose-decorated viscous guar gum galactomannan and crystalline ivory nut mannan at high enzyme concentrations, but the specific activity was fourfold to ninefold reduced at low enzyme and substrate concentrations compared with the enzyme lacking CBM10-2 and CBM10-3. Comparison of activity and binding data for the different enzyme forms indicates unproductive and productive polysaccharide binding to occur. We conclude that the C-terminal-most CBM10-3 secures firm binding, with contribution from CBM10-2, which with CBM10-1 also provides spatial flexibility. Interactions between proteins and carbohydrates play a vital role in life and have through evolution been optimized to match the environments where they take place. Affinities of protein–carbohydrate complexes range from millimolar to nanomolar. Low-affinity binding (millimolar range) is considered a key factor in dynamic systems, such as plant cell wall synthesis and degradation, microbe–host interplay, and synthesis and mobilization of storage polysaccharides. The carbohydrate active enzymes catalyzing these different reactions very often contain one or more noncatalytic carbohydrate-binding modules (CBMs) that facilitate the formation of enzyme–substrate complexes and can specifically bind with the substrate polysaccharides or with different polysaccharides located nearby, such as in the plant cell wall. It is common that polysaccharide hydrolases contain several CBMs, but it is difficult to understand the function of these individual CBMs because of their interplay with each other, substrate, other polysaccharides, and the catalytic domain (CD), and perhaps even more than one CD is present (1Conway J.M. Crosby J.R. Hren A.P. Southerland R.T. Lee L.L. Lunin V.V. Alahuhta P. Himmel M.E. Bomble Y.J. Adams M.W.W. Kelly R.M. Novel multidomain, multifunctional glycoside hydrolases from highly lignocellulolytic Caldicellulosiruptor species.Aiche J. 2018; 64: 4218-4228Crossref Scopus (11) Google Scholar). Certain insights are established, for example, on enzymes in cellulosomes with domains of the polyspecific CBM32 family interacting with galactose, lactose, polygalacturonic acid, and N-acetyllactosamine (2Low K.E. Smith S.P. Abbott D.W. Boraston A.B. 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Chem. 2016; 291: 7439-7449Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar). Typically, these enzymes have more than one CBM10 or contain also CBMs from other families, CBM2s being particularly common (Table 1).Table 1Summary of characteristics of enzymes having one or more CBM10(s)OrganismGenBank accession no.Modular organizationCBM10 bindingEnzymatic activityBinding-site residuesDisulphide bridgesRef.C. japonicusACE85176CBM10-GH26ND■◆DWF2(17Hogg D. Pell G. Dupree P. Goubet F. Marti S.M. Gilbert H.J. The modular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation.Biochemistry. 2003; 1043: 1027-1043Crossref Google Scholar)S. degradans (SdGH5CBM10-1)ABD79918GH5_8-CBM10-CBM10-CBM10■(Kd = 3.7 g/l) [◯•]■□◆SWY2C. japonicus (CjAA10CBM10)ACE84760AA10-CBM10◯(Kd = 7.5–17.3 μM)◯[•]YWN2(20Crouch L.I. Labourel A. Walton P.H. Davies G.J. Gilbert H.J. The contribution of non-catalytic carbohydrate binding modules to the activity of lytic polysaccharide monooxygenases.J. Biol. Chem. 2016; 291: 7439-7449Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar, 24Gardner J.G. Crouch L. Labourel A. Forsberg Z. Bukhman Y.V. Vaaje-Kolstad G. Gilbert H.J. Keating D.H. Systems biology defines the biological significance of redox-active proteins during cellulose degradation in an aerobic bacterium.Mol. Microbiol. 2014; 94: 1121-1133Crossref Scopus (37) Google Scholar)A. bacteriumAIF91534GH5_8-CBM10-CBM10-CBM10ND■YWY2(26O'Connor R.M. Fung J.M. Sharp K.H. Benner J.S. McClung C. Cushing S. Lamkin E.R. Fomenkov A.I. Henrissat B. Londer Y.Y. Scholz M.B. Posfai J. Malfatti S. Tringe S.G. Woyke T. et al.Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk.Proc. Natl. Acad. Sci. 2014; 111: E5096-E5104Crossref PubMed Scopus (55) Google Scholar)C. japonicusACE82655CBM5-CBM10-CBM35-GH5_7ND■□◆YWW2(17Hogg D. Pell G. Dupree P. Goubet F. Marti S.M. Gilbert H.J. The modular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation.Biochemistry. 2003; 1043: 1027-1043Crossref Google Scholar)C. japonicusACE82688CBM2-CBM10-GH45◯•▲YWY2(23Gilbert H.J. Hall J. Hazlewood G.P. Ferreira L.M.A. The N-terminal region of an endoglucanase from Pseudomonas fluorescens subspecies cellulosa constitutes a cellulose-binding domain that is distinct from the catalytic centre.Mol. Microbiol. 1990; 4: 759-767Crossref PubMed Scopus (66) Google Scholar)C. mixtusCAA88761GH11-CBM60-CE4-CBM10ND▲[•]WWW2(29Millward-Sadler S.J. Davidson K. Hazlewood G.P. Black G.W. Gilbert H.J. Clarke J.H. Novel cellulose-binding domains, NodB homologues and conserved modular architecture in xylanases from the aerobic soil bacteria Pseudomonas fluorescens subsp. cellulosa and Cellvibrio mixtus.Biochem. J. 1995; 312: 39-48Crossref PubMed Scopus (74) Google Scholar)A. bacteriumAIF91529CBM10-CBM10-GH10_4ND▲YWW2(26O'Connor R.M. Fung J.M. Sharp K.H. Benner J.S. McClung C. Cushing S. Lamkin E.R. Fomenkov A.I. Henrissat B. Londer Y.Y. Scholz M.B. Posfai J. Malfatti S. Tringe S.G. Woyke T. et al.Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk.Proc. Natl. Acad. Sci. 2014; 111: E5096-E5104Crossref PubMed Scopus (55) Google Scholar)C. japonicusACE84673GH5_8-CBM10-CBM10◯□[■•]■◆[□•]YWW2(17Hogg D. Pell G. Dupree P. Goubet F. Marti S.M. Gilbert H.J. The modular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation.Biochemistry. 2003; 1043: 1027-1043Crossref Google Scholar)C. japonicusACE85978CBM2-CBM10-GH6ND◯[•▲]YWW2(24Gardner J.G. Crouch L. Labourel A. Forsberg Z. Bukhman Y.V. Vaaje-Kolstad G. Gilbert H.J. Keating D.H. 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