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Characterization of the First Α-(1→ 3) Branching Sucrases of the GH70

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Characterization of the First Α-(1→ 3) Branching Sucrases of the GH70 Characterization of the First α-(1!3) Branching Sucrases of the GH70 Family Marlène Vuillemin, Marion Claverie, Yoann Brison, Etienne Séverac, Pauline Bondy, Sandrine Morel, Pierre Monsan, Claire Moulis, Magali Remaud Simeon To cite this version: Marlène Vuillemin, Marion Claverie, Yoann Brison, Etienne Séverac, Pauline Bondy, et al.. Char- acterization of the First α-(1!3) Branching Sucrases of the GH70 Family. Journal of Biological Chemistry, American Society for Biochemistry and Molecular Biology, 2016, 291 (14), pp.7687-7702. 10.1074/jbc.M115.688044. hal-01601907 HAL Id: hal-01601907 https://hal.archives-ouvertes.fr/hal-01601907 Submitted on 27 May 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Copyright crossmark THE JOURNAL OF BIOLOGICAL CHEMISTRY VOL. 291, NO. 14, pp. 7687–7702, April 1, 2016 © 2016 by The American Society for Biochemistry and Molecular Biology, Inc. Published in the U.S.A. Characterization of the First ␣-(133) Branching Sucrases of the GH70 Family*□S Received for publication, August 26, 2015, and in revised form, January 11, 2016 Published, JBC Papers in Press, January 13, 2016, DOI 10.1074/jbc.M115.688044 Marle`ne Vuillemin, Marion Claverie, Yoann Brison, Etienne Se´verac, Pauline Bondy, Sandrine Morel, Pierre Monsan, Claire Moulis1, and Magali Remaud-Sime´on2 From the Universite´ de Toulouse, Institut National des Sciences Applique´es (INSA), Universite´ Paul Sabatie´ (UPS), Institut National Polytechnique (INP), Laboratoire d’Inge´nieries des Syste`mes Biologiques et des Proce´de´s (LISBP), 135 Avenue de Rangueil, F-31077 Toulouse, France, CNRS, UMR5504, F-31400 Toulouse, France, and Institut National de la Recherche Agronomique (INRA), UMR792 Inge´nierie des Syste`mes Biologiques et des Proce´de´s, F-3140 Toulouse, France Leuconostoc citreum NRRL B-742 has been known for years to as a source of synthetic blood volume expanders (3). These produce a highly ␣-(133)-branched dextran for which the syn- findings motivated Jeanes et al. (22) to investigate the diversity thesis had never been elucidated. In this work a gene coding for of polymers produced during sucrose fermentation by different a putative ␣-transglucosylase of the GH70 family was identified strains of lactic acid bacteria. A total of 96 strains were in the reported genome of this bacteria and functionally charac- screened, and their dextrans were structurally characterized. In terized. From sucrose alone, the corresponding recombinant this study one strain, Leuconostoc mesenteroides NRRL B-742, protein, named BRS-B, mainly catalyzed sucrose hydrolysis and also known as L. mesenteroides ATCC 13146 and renamed Leu- leucrose synthesis. However, in the presence of sucrose and a conostoc citreum NRRL B-742 (4), received particular attention. dextran acceptor, the enzyme efficiently transferred the gluco- Indeed, this strain, first isolated from a can of spoiled tomatoes syl residue from sucrose to linear ␣-(136) dextrans through the in 1927 (1), was shown to produce two types of dextrans that specific formation of ␣-(133) linkages. To date, BRS-B is the differed by their structures and degree of solubility from first reported ␣-(133) branching sucrase. Using a suitable sucrose. The less soluble polymer contained 75% of ␣-(136) sucrose/dextran ratio, a comb-like dextran with 50% of ␣-(133) linkages and 15% of ␣-(134) linkages, whereas the more solu- branching was synthesized, suggesting that BRS-B is likely ble polymer displayed an uncommon comb-like structure con- involved in the comb-like dextran produced by L. citreum NRRL sisting of a linear backbone of ␣-(136)-D-glucopyranosyl resi- B-742. In addition, data mining based on the search for specific dues grafted with one ␣-(133)-linked glucosyl unit on every sequence motifs allowed the identification of two genes puta- glucosyl moiety (5–9). Concomitantly with those findings, dex- tively coding for branching sucrases in the genome of Leucono- trans were shown to be synthesized by ␣-transglucosylases, stoc fallax KCTC3537 and Lactobacillus kunkeei EFB6. Bio- commonly named glucansucrases, and today classified in the chemical characterization of the corresponding recombinant family 70 of glycoside hydrolases (GH70)3 (10). The GH70 fam- enzymes confirmed their branching specificity, revealing that ily belongs to the clan GH-H, together with families GH13 and branching sucrases are not only found in L. citreum species. GH77. To date, 279 ␣-transglucosylase sequences have been According to phylogenetic analyses, these enzymes are pro- reported in the CAZy database, and only 25% has been func- posed to constitute a new subgroup of the GH70 family. tionally characterized (11). Furthermore, only four three-di- mensional structures of GH70 enzymes have been solved (12– 15). The enzymes are organized into five different structural Numerous lactic acid bacteria from the Leuconostoc genus domains, A, B, C, IV, and V. The A, B, and C domains are related isolated from different habitats, such as sugar juice, fermenting to GH13 family enzymes, whereas domains IV and V are GH70- vegetables, or dairy products, have long been known to produce specific domains. The fold of these enzymes is unique, and slimes in sucrose solution (1, 2). These slimy compounds were except for domain C, all domains are formed by non-contigu- rapidly characterized as dextrans, homopolymers of ␣-D-gluco- ous fragments of sequences that assemble around a U-turn (15). ␣ pyranosyl units mainly linked by ␣-(136) linkages. Dextrans These enzymes are -retaining enzymes. They mainly catalyze ␣ with a high content of ␣-(136) linkages and a low degree of -transglucosylation reactions through a classical double dis- branching found their first industrial applications in the 1940s placement mechanism. The reaction starts with the formation of a ␤-D-glucosyl-enzyme intermediate involving a nucleophilic aspartate, an acid-base glutamic acid, and a third aspartate that * This work was supported by the French National Research Agency (ANR-12- CDII-0005, Engel 2012-2015) and the Re´gion Midi-Pyre´ne´es (France). The stabilizes the covalent intermediate. In a second step the inter- authors declare that they have no conflict of interest with the contents of mediate can be intercepted by a water molecule (hydrolysis this article. reaction) or by the hydroxyl group of an acceptor (transgluco- □S This article contains supplemental Tables S1–S4 and Figs. S1–S3. 1 To whom correspondence may be addressed: INSA, LISBP, 135 Avenue de Rangueil, F-31077 Toulouse, France. Tel.: 33-561-559-446; Fax: 33-561-559- 400; E-mail: [email protected]. 3 The abbreviations used are: GH, glycoside hydrolase; HPAEC-PAD, high per- 2 To whom correspondence may be addressed: INSA, LISBP, 135 Avenue de formance anion exchange chromatography with pulsed amperometric Rangueil, F-31077 Toulouse, France. Tel.: 33-561-559-446; Fax: 33-561-559- detection; HPSEC, high performance size exclusion chromatography; con- 400; E-mail: [email protected]. tig, group of overlapping clones. APRIL 1, 2016•VOLUME 291•NUMBER 14 JOURNAL OF BIOLOGICAL CHEMISTRY 7687 First ␣-(133) Branching Sucrases from the GH70 Family SCHEME 1. Main reactions catalyzed by GH70 sucrose-active enzymes. sylation). The synthesis of the polymer occurs via successive ␣-(134) linkages was isolated, the enzyme contributing to the transfers of glucosyl units onto the non-reducing extremity of comb-like structure was never identified (5). Of note, most of the growing ␣-glucan chain (Scheme 1) (16–18). the GH70 enzyme activities were found strongly attached to the Among GH70 sucrose-active enzymes, four subgroups of cell wall, making the enzymes difficult to purify (7). Crude glucansucrases can be distinguished: the dextransucrases, enzyme extracts or sucrose fermentation broths were thus used alternansucrases, mutansucrases, and reuteransucrases, which to produce ␣-(133)-branched glucooligosaccharides from are all efficient polymerases (10). In addition, one branching sucrose and maltose (7), and these compounds were shown to sucrase (GBD-CD2) was engineered from L. citreum NRRL possess interesting functional properties. In particular, they B-1299 DSR-E dextransucrase (19). This enzyme displays no stimulated in vitro growth of beneficial bacteria such as bifido- polymerase activity but catalyzes ␣-(136) dextran branching bacteria or lactobacilli and inhibited the development of patho- very efficiently with single ␣-(132)-linked glucosyl units gens such as Salmonella sp. or Escherichia coli (23, 24). In 2000, (Scheme 1) (20). Recently, genome sequencing of L. citreum Kim and Robyt (25) cloned a gene from the mutant strain L. cit- NRRL B-1299 allowed the identification of the first natural reum NRRL B-742CB. The encoded protein, DSR-B-742, ␣-(132) branching sucrase, BRS-A, that shows the same spec- shared Ͼ95% amino acid identity with DSR-B dextransucrase ificity as GBD-CD2. This enzyme was proposed to be involved from L. citreum NRRL B-1299 and synthesized a quasilinear in the formation of the native dextrans of L. citreum NRRL dextran with Ͼ95% of ␣-(136) linkages (26). Thus far the mode B-1299 that contain a high percentage of ␣-(132) linkages of synthesis of the comb-like dextran has remained unknown. (21, 22). A genomic approach was undertaken to gain insight into the The formation of the regular hyper-branched dextran of formation of this hyper-branched ␣-glucan and to have access L. citreum NRRL B-742 is even more intriguing. Several to enzymatic tools of interest for functional glucooligosaccha- attempts to isolate the GH70 enzymes of L. citreum NRRL ride synthesis. First, the genome of L. citreum NRRL B-742 was B-742 were reported.
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