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Structure-Function Relationships of Glucansucrase and Fructansucrase Enzymes from Lactic Acid Bacteria Sacha A

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Structure-Function Relationships of Glucansucrase and Fructansucrase Enzymes from Lactic Acid Bacteria Sacha A MICROBIOLOGY AND MOLECULAR BIOLOGY REVIEWS, Mar. 2006, p. 157–176 Vol. 70, No. 1 1092-2172/06/$08.00ϩ0 doi:10.1128/MMBR.70.1.157–176.2006 Copyright © 2006, American Society for Microbiology. All Rights Reserved. Structure-Function Relationships of Glucansucrase and Fructansucrase Enzymes from Lactic Acid Bacteria Sacha A. F. T. van Hijum,1,2†* Slavko Kralj,1,2† Lukasz K. Ozimek,1,2 Lubbert Dijkhuizen,1,2 and Ineke G. H. van Geel-Schutten1,3 Centre for Carbohydrate Bioprocessing, TNO-University of Groningen,1 and Department of Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen,2 9750 AA Haren, The Netherlands, and Innovative Ingredients and Products Department, TNO Quality of Life, Utrechtseweg 48 3704 HE Zeist, The Netherlands3 Downloaded from INTRODUCTION .......................................................................................................................................................157 NOMENCLATURE AND CLASSIFICATION OF SUCRASE ENZYMES ........................................................158 GLUCANSUCRASES .................................................................................................................................................158 Reactions Catalyzed and Glucan Product Synthesis .........................................................................................161 Glucan synthesis .................................................................................................................................................161 Acceptor reaction ................................................................................................................................................161 Structural and Functional Organization of Glucansucrase Enzymes.............................................................161 Signal peptide and N-terminal variable domain............................................................................................162 Catalytic domain.................................................................................................................................................163 (i) Catalytic residues ......................................................................................................................................163 http://mmbr.asm.org/ (ii) Catalytic site .............................................................................................................................................164 (iii) Amino acid substitutions .......................................................................................................................164 C-terminal domain..............................................................................................................................................165 Reaction Mechanism of Glucansucrase Enzymes ..............................................................................................166 FRUCTANSUCRASES ...............................................................................................................................................167 Reactions Catalyzed and Fructan Product Synthesis........................................................................................167 Fructan synthesis................................................................................................................................................167 Fructo-oligosaccharide synthesis ......................................................................................................................167 Structural and Functional Organization of Fructansucrase Enzymes............................................................167 Signal peptide and N-terminal variable domain............................................................................................168 Catalytic domain.................................................................................................................................................168 on September 22, 2019 by guest (i) Catalytic residues ......................................................................................................................................168 (ii) Catalytic site .............................................................................................................................................169 (iii) Mutations affecting product formation................................................................................................169 (iv) Calcium binding site ...............................................................................................................................170 C-terminal domain..............................................................................................................................................170 Reaction Mechanism of Fructansucrase Enzymes.............................................................................................170 Putative Fructansucrases in Lactic Acid Bacteria .............................................................................................170 CONCLUSIONS AND FUTURE DIRECTIONS....................................................................................................171 ACKNOWLEDGMENTS ...........................................................................................................................................171 REFERENCES ............................................................................................................................................................171 INTRODUCTION transferase enzymes (39). In contrast, homopolysaccharides are synthesized from the sole substrate sucrose by the action of Extracellular polysaccharides (exopolysaccharides) (EPS) one sucrase enzyme. Sucrase-type enzymes synthesize polysac- are commonly found in bacteria and microalgae and less fre- charides consisting of either glucose sugar residues (glucans) quently in yeasts and fungi (39, 142, 160, 168, 217). Several lactic acid bacteria (LAB), including species of Lactobacillus, or fructose residues (fructans). are known to produce EPS. Depending on their composition Homopolysaccharide synthesis in LAB has mainly been and mechanism of biosynthesis, EPS are divided in two classes: studied in oral streptococci and Leuconostoc spp. (124, 126, heteropolysaccharides and homopolysaccharides. Heteropoly- 149, 153). Because of their clearly established role in formation saccharides consist of multiple sugar types and are synthesized of dental caries (7) Streptococcus mutans and Streptococcus by the combined action of multiple different types of glycosyl- sanguis strains have been subject to a number of studies (18, 100, 109, 157, 159). Interestingly, there is increasing evidence that a number of Lactobacillus species are also associated with * Corresponding author. Present address: Department of Molecular advanced stages of dental caries (26). Both glucans and fruc- Genetics, Groningen Biomolecular Sciences and Biotechnology Insti- tans (see below) formed by oral streptococci (and lactobacilli) tute, University of Groningen, P.O. Box 14, 9750 AA Haren, The apparently have major influences on the formation of dental Netherlands. Phone: 31.50.3632415. Fax: 31.50.3632154. E-mail: s.a.f [email protected]. plaque. They are involved in adherence of bacteria to each † These authors contributed equally to the work. other and to the tooth surface, modulating diffusion of sub- 157 158 VAN HIJUM ET AL. MICROBIOL.MOL.BIOL.REV. stances through plaque, and occasionally serving as extracellu- nature for enzymes that catalyze the transfer of, for instance, lar energy reserves (29, 41, 141, 162). Alternatively, these poly- glucosyl and fructosyl sugar units, they are not descriptive for mers may protect microbial cells against desiccation, phagocytosis the substrate and product specificity of sucrase-type enzymes. and phage attack, antibiotics or toxic compounds, predation by Therefore, in this review we only use glucansucrases and fruc- protozoans, and osmotic stress (20). tansucrases for enzymes synthesizing homopolysaccharides In general, glucans and/or fructans can be used as viscosify- from sucrose. ing, stabilizing, emulsifying, sweetening, gelling, or water-bind- In another classification system, glycoside hydrolase (GH) ing agents, in the food as well as in the nonfood industries (40, enzymes have been divided into 100 different families based on 51, 66, 190, 217, 218). Certain oligosaccharides (e.g., fructo- their amino acid sequences (33; http://afmb.cnrs-mrs.fr/CAZY/). oligosaccharides, isomaltooligosaccharides, and lactulose) and In view of their (different) sequence similarities, GS and FS polysaccharides (e.g., fructans) are used as prebiotic food ad- have been included in the families GH70 and GH68, respec- ditives (14, 15, 50, 84, 151, 164). Additionally, oligosaccharides tively. Evolutionarily, structurally, and mechanistically related Downloaded from containing ␣-(132) glucosidic bonds are in some cases used as families are further grouped into clans. Enzymes from the feed additives (127). families GH32 (consisting mainly of plant and fungal fructo- Over the years a large number of glucansucrase and fruc- syltransferases) and GH68 comprise clan GH-J. The members tansucrase genes and enzymes have been identified by cloning, of clan GH-J possess a five-bladed ␤-propeller structure (33; reverse genetics, and various enzyme activity assays. Enzymes http://afmb.cnrs-mrs.fr/CAZY/), with three identical catalytic synthesizing ␣-glucan
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