Inventory of the GH70 enzymes encoded by Leuconostoc citreum NRRL B-1299 - Identification of three novel α-transglucosylases

FEBS Journal

Volumn 282, Issue 11, 2015, Pages 2115-2130

  Passerini, Delphine ^a,b,c   Vuillemin, Marlène ^a,b,c   Ufarté, Lisa ^a,b,c   Morel, Sandrine ^a,b,c   Loux, Valentin ^d   Fontagné Faucher, Catherine ^e   Monsan, Pierre ^a,b,c   Remaud Siméon, Magali ^a,b,c,f   Moulis, Claire ^a,b,c  

^a INSA   (France)

^b CNRS   (France)

^c UMR792 INGÉNIERIE DES SYSTÈMES BIOLOGIQUES ET DES PROCÉDÉS   (France)

^d CEMAGREF   (France)

^e Université Paul Sabatier   (France)

^f UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

branching sucrase; dextransucrase; glucansucrase; Leuconostoc citreum NRRL B 1299; transglucosylase

Indexed keywords

BACTERIAL ENZYME; DEXTRAN; GH70 ENZYME; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; DEXTRANSUCRASE; GLUCOSYLTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BIOCHEMISTRY; BRSA GENE; CONTROLLED STUDY; DSRDP GENE; DSRM GENE; GENE DUPLICATION; GENE IDENTIFICATION; GENE SEQUENCE; GENE TRANSFER; LEUCONOSTOC; LEUCONOSTOC CITREUM; NONHUMAN; PRIORITY JOURNAL; PROPHAGE; SEQUENCE ANALYSIS; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; KINETICS; MOLECULAR GENETICS; PH;

LEUCONOSTOC CITREUM;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; GLUCOSYLTRANSFERASES; HYDROGEN-ION CONCENTRATION; KINETICS; LEUCONOSTOC; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; SUBSTRATE SPECIFICITY;

EID: 84930667927     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13261     Document Type: Article

References (65)

1. Naessens M, Cerdobbel A, Soetaert W, &, Vandamme EJ, (2005) Leuconostoc dextransucrase and dextran: production, properties and applications. J Chem Technol Biotechnol 80, 845-860.
2. Freitas F, Alves VD, &, Reis MAM, (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol 29, 388-398.
3. Badel S, Bernardi T, &, Michaud P, (2011) New perspectives for Lactobacilli exopolysaccharides. Biotechnol Adv 29, 54-66.
4. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, &, Henrissat B, (2013) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42, 490-495.
5. Leemhuis H, Pijning T, Dobruchowska JM, van Leeuwen SS, Kralj S, Dijkstra BW, &, Dijkhuizen L, (2013) Glucansucrases: three-dimensional structures, reactions, mechanism, α-glucan analysis and their implications in biotechnology and food applications. J Biotechnol 163, 250-272.
6. Devulapalle KS, Goodman SD, Gao Q, Hemsley A, &, Mooser G, (1997) Knowledge-based model of a glucosyltransferase from the oral bacterial group of mutans streptococci. Protein Sci 6, 2489-2493.
7. van Hijum SAFT, Kralj S, Ozimek LK, Dijkhuizen L, &, van Geel-Schutten IGH, (2006) Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol Mol Biol Rev 70, 157-176.
8. Vujičic-Žagar A, Pijning T, Kralj S, López CA, Eeuwema W, Dijkhuizen L, &, Dijkstra BW, (2010) Crystal structure of a 117 kDa glucansucrase fragment provides insight into evolution and product specificity of GH70 enzymes. Proc Natl Acad Sci USA 107, 21406-21411.
9. Ito K, Ito S, Shimamura T, Weyand S, Kawarasaki Y, Misaka T, Abe K, Kobayashi T, Cameron AD, &, Iwata S, (2011) crystal structure of glucansucrase from the dental caries pathogen Streptococcus mutans. J Mol Biol 408, 177-186.
10. Brison Y, Pijning T, Malbert Y, Fabre E, Mourey L, Morel S, Potocki-Veronese G, Monsan P, Tranier S, Remaud-Simeon M, et al,. (2012) Functional and structural characterization of α-1,2 branching sucrase derived from DSR-E glucansucrase. J Biol Chem 287, 7915-7924.
11. Pijning T, Vujičic-Žagar A, Kralj S, Dijkhuizen L, &, Dijkstra BW, (2012) Structure of the α-1,6/α-1,4-specific glucansucrase GTFA from Lactobacillus reuteri 121. Acta Crystallogr 68, F1448-F1454.
12. MacGregor EA, Jespersen HM, &, Svensson B, (1996) A circularly permuted α-amylase-type α/β-barrel structure in glucan-synthesizing glucosyltransferases. FEBS Lett 378, 263-266.
13. Monchois V, (1999) Glucansucrases: mechanism of action and structure-function relationships. FEMS Microbiol Rev 23, 131-151.
14. Moulis C, Joucla G, Harrison D, Fabre E, Potocki-Veronese G, Monsan P, &, Remaud-Simeon M, (2006) Understanding the polymerization mechanism of glycoside-hydrolase family 70 glucansucrases. J Biol Chem 281, 31254-31267.
15. Giffard PM, &, Jacques NA, (1994) Definition of a fundamental repeating unit in streptococcal glucosyltransferase glucan-binding regions and related sequences. J Dent Res 73, 1133-1141.
16. Jeanes A, Haynes WC, Wilham CA, Rankin JC, Melvin EH, Austin MJ, Cluskey JE, Fisher BE, Tsuchiya HM, &, Rist CE, (1954) Characterization and classification of dextrans from ninety-six strains of bacteria 1b. J Am Chem Soc 76, 5041-5052.
17. Brooker BE, (1977) Ultrastructural surface changes associated with dextran synthesis by Leuconostoc mesenteroides. J Bacteriol 131, 288-292.
18. Kobayashi M, &, Matsuda K, (1977) Structural characteristics of dextrans synthesized by dextransucrases from Leuconostoc mesenteroides NRRL B-1299. Agric Biol Chem 41, 1931-1937.
19. Sarbini SR, Kolida S, Naeye T, Einerhand A, Brison Y, Remaud-Simeon M, Monsan P, Gibson GR, &, Rastall RA, (2011) In vitro fermentation of linear and α-1,2-branched dextrans by the human fecal microbiota. Appl Environ Microbiol 77, 5307-5315.
20. Sarbini SR, Kolida S, Naeye T, Einerhand AW, Gibson GR, &, Rastall RA, (2013) The prebiotic effect of α-1,2 branched, low molecular weight dextran in the batch and continuous faecal fermentation system. J Funct Foods 5, 1938-1946.
21. Bounaix M-S, Gabriel V, Robert H, Morel S, Remaud-Siméon M, Gabriel B, &, Fontagné-Faucher C, (2010) Characterization of glucan-producing Leuconostoc strains isolated from sourdough. Int J Food Microbiol 144, 1-9.
22. Monchois V, Willemot R-M, Remaud-Simeon M, Croux C, &, Monsan P, (1996) Cloning and sequencing of a gene coding for a novel dextransucrase from Leuconostoc mesenteroides NRRL B-1299 synthesizing only α(1-6) and α(1-3) linkages. Gene 182, 23-32.
23. Monchois V, (1998) Cloning and sequencing of a gene coding for an extracellular dextransucrase (DSRB) from Leuconostoc mesenteroides NRRL B-1299 synthesizing only a α(1-6) glucan. FEMS Microbiol Lett 159, 307-315.
24. Bozonnet S, Dols-Laffargue M, Fabre E, Pizzut S, Remaud-Simeon M, Monsan P, &, Willemot R-M, (2002) Molecular characterization of DSR-E, an α-1,2 linkage-synthesizing dextransucrase with two catalytic domains. J Bacteriol 184, 5753-5761.
25. Fabre E, Bozonnet S, Arcache A, Willemot R-M, Vignon M, Monsan P, &, Remaud-Simeon M, (2005) Role of the two catalytic domains of DSR-E dextransucrase and their involvement in the formation of highly α-1,2 branched dextran. J Bacteriol 187, 296-303.
26. Kim D, &, Robyt JF, (1995) Dextransucrase constitutive mutants of Leuconostoc mesenteroides B-1299. Enzyme Microb Technol 17, 1050-1056.
27. Liu Y, Harrison PM, Kunin V, &, Gerstein M, (2004) Comprehensive analysis of pseudogenes in prokaryotes: widespread gene decay and failure of putative horizontally transferred genes. Genome Biol 5, R64.
28. Siguier P, Perochon J, Lestrade L, Mahillon J, &, Chandler M, (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34, D32-D36.
29. Kim JF, Jeong H, Lee J-S, Choi S-H, Ha M, Hur C-G, Kim J-S, Lee S, Park H-S, Park Y-H, et al,. (2008) Complete genome sequence of Leuconostoc citreum KM20. J Bacteriol 190, 3093-3094.
30. Laguerre S, Amari M, Vuillemin M, Robert H, Loux V, Klopp C, Morel S, Gabriel B, Remaud-Siméon M, Gabriel V, et al,. (2012) Genome sequences of three Leuconostoc citreum strains, LBAE C10, LBAE C11, and LBAE E16, isolated from wheat sourdoughs. J Bacteriol 194, 1610-1611.
31. Passerini D, Vuillemin M, Laguerre S, Amari M, Loux V, Gabriel V, Robert H, Morel S, Monsan P, Gabriel B, et al,. (2014) Complete genome sequence of Leuconostoc citreum strain NRRL B-742. Genome Announc 2, e01179-14.
32. Mahony J, Ainsworth S, Stockdale S, &, van Sinderen D, (2012) Phages of lactic acid bacteria: the role of genetics in understanding phage-host interactions and their co-evolutionary processes. Virology 434, 143-150.
33. Lu Z, Altermann E, Breidt F, &, Kozyavkin S, (2010) Sequence analysis of Leuconostoc mesenteroides bacteriophage 1-A4 isolated from an industrial vegetable fermentation. Appl Environ Microbiol 76, 1955-1966.
34. Kleppen HP, Nes IF, &, Holo H, (2012) Characterization of a Leuconostoc bacteriophage infecting flavor producers of cheese starter cultures. Appl Environ Microbiol 78, 6769-6772.
35. Ali Y, Kot W, Atamer Z, Hinrichs J, Vogensen FK, Heller KJ, &, Neve H, (2013) Classification of lytic bacteriophages attacking dairy Leuconostoc starter strains. Appl Environ Microbiol 79, 3628-3636.
36. Zhou Y, Liang Y, Lynch KH, Dennis JJ, &, Wishart DS, (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39, W347-W352.
37. Brison Y, Fabre E, Moulis C, Portais J-C, Monsan P, &, Remaud-Siméon M, (2009) Synthesis of dextrans with controlled amounts of α-1,2 linkages using the transglucosidase GBD-CD2. Appl Microbiol Biotechnol 86, 545-554.
38. Amari M, Gabriel V, Robert H, Morel S, Moulis C, Gabriel B, Remaud-Siméon M, &, Fontagné-Faucher C, (2014) Overview of the glucansucrase equipment of Leuconostoc citreum LBAE-E16 and LBAE-C11, two strains isolated from sourdough. FEMS Microbiol Lett, 362, 1-8.
39. Argüello-Morales MA, Remaud-Simeon M, Pizzut S, Sarçabal P, Willemot R, &, Monsan P, (2000) Sequence analysis of the gene encoding alternansucrase, a sucrose glucosyltransferase from Leuconostoc mesenteroides NRRL B-1355. FEMS Microbiol Lett 182, 81-85.
40. Olivares-Illana V, López-Munguía A, &, Olvera C, (2003) Molecular characterization of inulosucrase from Leuconostoc citreum: a fructosyltransferase within a glucosyltransferase. J Bacteriol 185, 3606-3612.
41. Moulis C, Arcache A, Escalier P-C, Rinaudo M, Monsan P, Remaud-Simeon M, &, Potocki-Veronese G, (2006) High-level production and purification of a fully active recombinant dextransucrase from Leuconostoc mesenteroides NRRL B-512F. FEMS Microbiol Lett 261, 203-210.
42. Jung JY, Lee SH, &, Jeon CO, (2012) Complete genome sequence of Leuconostoc carnosum strain JB16, isolated from kimchi. J Bacteriol 194, 6672-6673.
43. Jung JY, Lee SH, Lee SH, &, Jeon CO, (2012) Complete genome sequence of Leuconostoc mesenteroides subsp. mesenteroides strain J18, isolated from kimchi. J Bacteriol 194, 730-731.
44. Lee SH, Jung JY, Lee SH, &, Jeon CO, (2011) Complete genome sequence of Leuconostoc kimchii strain C2, isolated from kimchi. J Bacteriol 193, 5548-5548.
45. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, et al,. (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103, 15611-15616.
46. Bourne EJ, Sidebotham RL, &, Weigel H, (1972) Studies on dextrans and dextranases: part X. Types and percentages of secondary linkages in the dextrans elaborated by Leuconostoc mesenteroides NRRL B-1299. Carbohydr Res 22, 13-22.
47. Seymour FR, Slodki ME, Plattner RD, &, Jeanes A, (1977) Six unusual dextrans: methylation structural analysis by combined g.l.c.-m.s. of per-O-acetyl-aldononitriles. Carbohydr Res 53, 153-166.
48. Watanabe T, Shishido K, Kobayashi M, &, Matsuda K, (1978) Acetolysis of Leuconostoc mesenteroides NRRL B-1299 dextran. Isolation and characterization of tetrasacharrides containing secondary linkages from the borate-insoluble fraction. Carbohydr Res 61, 119-128.
49. Dols M, Remaud-Simeon M, Willemot RM, Vignon M, &, Monsan P, (1998) Characterization of the different dextransucrase activities excreted in glucose, fructose, or sucrose medium by Leuconostoc mesenteroides NRRL B-1299. Appl Environ Microbiol 64, 1298-1302.
50. Monchois V, Reverte A, Remaud-Simeon M, Monsan P, &, Willemot R-M, (1998) Effect of Leuconostoc mesenteroides NRRL B-512F dextransucrase carboxy-terminal deletions on dextran and oligosaccharide synthesis. Appl Environ Microbiol 64, 1644-1649.
51. Moulis C, Vaca Medina G, Suwannarangsee S, Monsan P, Remaud-Simeon M, &, Potocki-Veronese G, (2008) One-step synthesis of isomalto-oligosaccharide syrups and dextrans of controlled size using engineered dextransucrase. In Biocatalysis and biotransformation pp. 141-151. Taylor & Francis, Abingdon, UK.
52. Kralj S, van Geel-Schutten IGH, Faber EJ, van der Maarel MJEC, &, Dijkhuizen L, (2005) Rational transformation of Lactobacillus reuteri 121 reuteransucrase into a dextransucrase. Biochemistry 44, 9206-9216.
53. Hoshino T, Fujiwara T, &, Kawabata S, (2012) Evolution of cariogenic character in Streptococcus mutans: horizontal transmission of glycosyl hydrolase family 70 genes. Sci Rep 2, 518.
54. Argimón S, Alekseyenko AV, DeSalle R, &, Caufield PW, (2013) Phylogenetic analysis of glucosyltransferases and implications for the coevolution of mutans Streptococci with their mammalian hosts. PLoS One 8, e56305.
55. Kralj S, van Geel-Schutten GH, Dondorff MMG, Kirsanovs S, van der Maarel MJEC, &, Dijkhuizen L, (2004) Glucan synthesis in the genus Lactobacillus: isolation and characterization of glucansucrase genes, enzymes and glucan products from six different strains. Microbiology 150, 3681-3690.
56. Bryson K, Loux V, Bossy R, Nicolas P, Chaillou S, van de Guchte M, Penaud S, Maguin E, Hoebeke M, Bessières P, et al,. (2006) AGMIAL: implementing an annotation strategy for prokaryote genomes as a distributed system. Nucleic Acids Res 34, 3533-3545.
57. Grant JR, &, Stothard P, (2008) The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res 36, W181-W184.
58. Darling AE, Mau B, &, Perna NT, (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5, e11147.
59. Tamura K, Stecher G, Peterson D, Filipski A, &, Kumar S, (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30, 2725-2729.
60. Castresana J, (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17, 540-552.
61. De Jong A, Pietersma H, Cordes M, Kuipers OP, &, Kok J, (2012) PePPER: a webserver for prediction of prokaryote promoter elements and regulons. BMC Genom 13, 299.
62. McCracken A, Turner MS, Giffard P, Hafner LM, &, Timms P, (2000) Analysis of promoter sequences from Lactobacillus and Lactococcus and their activity in several Lactobacillus species. Arch Microbiol 173, 383-389.
63. Chopin A, Bolotin A, Sorokin A, Ehrlich SD, &, Chopin M-C, (2001) Analysis of six prophages in Lactococcus lactis IL1403: different genetic structure of temperate and virulent phage populations. Nucleic Acids Res 29, 644-651.
64. Studier FW, (2005) Protein production by auto-induction in high-density shaking cultures. Protein Expr Purif 41, 207-234.
65. Miller GL, (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31, 426-428.