Characterization of structure/prebiotic potential correlation of glucans and oligosaccharides synthetized by glucansucrases from fructophilic lactic acid bacteria from honey bee Apis mellifera

References

• Berrios P, Fuentes JA, Salas D, et al. Inhibitory effect of biofilm-forming Lactobacillus kunkeei strains against virulent Pseudomonas aeruginosa in vitro and in honeycomb moth (Galleria mellonella) infection model. Benef Microbes. 2018;9(2):257–268.
   PubMed Web of Science ®Google Scholar
• Pachla A, Wicha M, Ptaszyńska AA, et al. The molecular and phenotypic characterization of fructophilic lactic acid bacteria isolated from the guts of Apis mellifera L. derived from a Polish apiary. J Appl Genet. 2018;59(4):503–514.
   PubMed Web of Science ®Google Scholar
• Khan KA, Al-Ghamdi AA, Ghramh HA, et al. Structural diversity and functional variability of gut microbial communities associated with honey bees. Microb Pathog. 2020; 138:103793.
   PubMed Web of Science ®Google Scholar
• Romero S, Nastasa A, Chapman A, et al. The honey bee gut microbiota: strategies for study and characterization. Insect Mol Biol. 2019;28(4):455–472.
   PubMed Web of Science ®Google Scholar
• Vuillemin M, Claverie M, Brison Y, et al. Characterization of the first α-(1→3) branching sucrases of the GH70 family. J Biol Chem. 2016;291(14):7687–7702.
   PubMed Web of Science ®Google Scholar
• Endo A. Fructophilic lactic acid bacteria inhabit fructose-rich niches in nature. Microb Ecol Health D. 2012; 23(18563):6–9.
   Google Scholar
• Olofsson TC, Vasquez A . Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Curr Microbiol. 2008;57(4):356–363.
   PubMed Web of Science ®Google Scholar
• Endo A, Futagawa-Endo Y, Dicks LMT. Isolation and characterization of fructophilic lactic acid bacteria from fructose-rich niches. Syst Appl Microbiol. 2009;32(8):593–600.
   PubMed Web of Science ®Google Scholar
• Endo A, Okada S . Reclassification of the genus Leuconostoc and proposals of Fructobacillus fructosus gen. nov., comb. nov., Fructobacillus durionis comb. nov., Fructobacillus ficulneus comb. nov. and Fructobacillus pseudoficulneus comb. nov. Int J Syst Evol Microbiol. 2008;58(Pt 9):2195–2205.
   PubMedGoogle Scholar
• Endo A, Futagawa-Endo Y, Sakamoto M, et al. Lactobacillus florum sp. nov., a fructophilic species isolated from flowers. Int J Syst Evol Microbiol. 2010;60(Pt 10):2478–2482.
   PubMedGoogle Scholar
• Neveling DP, Endo A, Dick LMT. Fructophilic Lactobacillus kunkeei and Lactobacillus brevis isolated from fresh flowers, bees and bee-hives. Curr Microbiol. 2012;65(5):507–515.
   PubMed Web of Science ®Google Scholar
• Endo A, Irisawa T, Futagawa-Endo Y, et al. Characterization and emended description of Lactobacillus kunkeei as a fructophilic lactic acid bacterium. Int J Syst Evol Microbiol. 2012;62(Pt 3):500–504.
   PubMedGoogle Scholar
• Monsan P, Bozonnet S, Albenne C, et al. Homopolysaccharides from lactic acid bacteria. Int Dairy J. 2001;11(9):675–685.
   Web of Science ®Google Scholar
• Naessens M, Cerdobbel A, Soetaert W, et al. Leuconostoc dextransucrase and dextran: production, properties and applications. J Chem Technol Biotechnol. 2005;80(8):845–860.
   Web of Science ®Google Scholar
• Zannini E, Waters DM, Coffey A, et al. Production, properties, and industrial food application of lactic acid bacteria-derived exopolysaccharides. Appl Microbiol Biotechnol. 2016;100(3):1121–1135.
   PubMed Web of Science ®Google Scholar
• Zeidan AA, Poulsen VK, Janzen T, et al. Polysaccharide production by lactic acid bacteria: from genes to industrial applications. FEMS Microbiol Rev. 2017;41(Supp_1):S168–S200.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Cui Y, Qu X. Exopolysaccharides of lactic acid bacteria: structure, bioactivity and associations: a review. Carbohydr Polym. 2019; 207:317–332.
   PubMed Web of Science ®Google Scholar
• Korakli M, Vogel RF . Structure/function relationship of homopolysaccharide producing glycansucrases and therapeutic potential of their synthesised glycans. Appl Microbiol Biotechnol. 2006;71(6):790–803.
   PubMed Web of Science ®Google Scholar
• van Hijum SAFT, Kralj S, Ozimek LK, et al. Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol Mol Biol Rev. 2006;70(1):157–176.
   PubMed Web of Science ®Google Scholar
• Gangoiti J, Pijning T, Dijkhuizen L. Biotechnological potential of novel glycoside hydrolase family 70 enzymes synthesizing α-glucans from starch and sucrose. Biotechnol Adv. 2018;36(1):196–207.
   PubMed Web of Science ®Google Scholar
• Monsan P, Remaud-Siméon M, André I. Transglucosidases as efficient tools for oligosaccharide and glucoconjugate synthesis. Curr Opin Microbiol. 2010;13(3):293–300.
   PubMed Web of Science ®Google Scholar
• Andre I, Potocki-Veronese G, Morel S. Sucrose-utilizing transglucosidases for biocatalysis. Top Curr Chem. 2010; 294:25–48.
   PubMed Web of Science ®Google Scholar
• Patel S, Goyal A. Functional oligosaccharides: production, properties and applications. World J Microbiol Biotechnol. 2011;27(5):1119–1128.
   Web of Science ®Google Scholar
• Monsan PF, Ouarne F. Oligosaccharides derived from sucrose. In: Charalampopoulos D, Rastall RA, editors. Prebiotics and Probiotics Science. New York: Springer Science + Media, 2009. p. 293–337.
   Google Scholar
• Monchois V, Remaud-Simeon M, Russell RR, et al. Characterization of Leuconostoc mesenteroides NRRL B-512F dextransucrase (DSRS) and identification of amino-acid residues playing a key role in enzyme activity. Appl Microbiol Biotechnol. 1997;48(4):465–472.
   PubMed Web of Science ®Google Scholar
• Fabre E, Bozonnet S, Arcache A, et al. Role of the two catalytic domains of DSR-E dextransucrase and their involvement in the formation of highly alpha-1,2 branched dextran. J Bacteriol. 2005;187(1):296–303.
   PubMed Web of Science ®Google Scholar
• Cote GL, Sheng S, Dunlap CA. Alternansucrase acceptor products. Biocatal Biotransfor. 2008;26(1-2):161–168.
   Web of Science ®Google Scholar
• Kralj S, van Geel-Schutten GH, van der Maarel MJEC, et al. Biochemical and molecular characterization of Lactobacillus reuteri 121 reuteransucrase. Microbiology (Reading)). 2004;150(Pt 7):2099–2112.
   PubMed Web of Science ®Google Scholar
• Vasileva T, Bivolarski V, Michailova G, et al. Glucansucrases produced by fructophilic lactic acid bacteria Lactobacillus kunkeei H3 and H25 isolated from honeybees. J Basic Microbiol. 2017;57(1):68–77.
   PubMed Web of Science ®Google Scholar
• Rabadjiev YK. Study of the genus Lactobacillus and the genus Fructobacillus in the microbiota of honey bees PhD dissertation, Sofia (Bulgaria): Sofia University “St. Kliment Ohridski”, 2018.
   Google Scholar
• Dols M, Remaud-Simeon M, Monsan PF. Dextransucrase production by Leuconostoc mesenteroides NRRL B-1299. Comparioson with L. mesenteroides NRRL B-512F. Enzyme Microb Technol. 1997;20(7):523–530.
   Web of Science ®Google Scholar
• Goyal A, Katiyar S. Fractionation of Leuconostoc mesenteroides NRRL B-512F dextransucrase by polyethylene glycol: a simple and effective method purification. J Microbiol Methods. 1994;20(3):225–231.
   Web of Science ®Google Scholar
• Miller GL. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem. 1959;31(3):426–429.
   Web of Science ®Google Scholar
• Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248–254.
   PubMed Web of Science ®Google Scholar
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680–685.
   PubMed Web of Science ®Google Scholar
• Miller AW, Robyt J. Detection of dextransucrase and levansucrase on polyacrylamide gels by the periodic acid-Schiff stain: staining artifacts and their prevention. Anal Biochem. 1986;156(2):357–363.
   PubMed Web of Science ®Google Scholar
• Bivolarski V, Vasileva T, Gabriel V, et al. Synthesis of glucooligosaccharides with prebiotic potential by glucansucrase URE 13-300 acceptor reactions with maltose, raffinose and lactose. Eng Life Sci. 2018;18(12):904–913.
   PubMed Web of Science ®Google Scholar
• Vasileva T, Iliev I, Amari M, et al. Characterization of glycosyltransferase activity of wild-type Leuconostoc mesenteroides strains from Bulgarian fermented vegetables. Appl Biochem Biotechnol. 2012;168(3):718–730.
   PubMed Web of Science ®Google Scholar
• Remaud M, Paul F, Monsan P, et al. Characterization of α-(1,3) branched oligosaccharides synthesized by acceptor reaction with the extracellular glucosyltransferase from L. mesenteroides NRRL B-742. J Carbohydr Chem. 1992;11(3):359–378.
   Web of Science ®Google Scholar
• Olvera C, Centeno-Leija S, López-Munguía A. Structural and functional features of fructansucrases present in Leuconostoc mesenteroides ATCC 8293. Antonie Van Leeuwenhoek. 2007;92(1):11–20.
   PubMed Web of Science ®Google Scholar
• Bounaix M-S, Gabriel V, Morel S, et al. Biodiversity of exopolysaccharides produced from sucrose by sourdough lactic acid bacteria. J Agric Food Chem. 2009;57(22):10889–10897.
   PubMed Web of Science ®Google Scholar
• Ananieva M, Tzenova M, Iliev I, et al. Gene expression of enzymes involved in utilization of xylooligosaccharides by Lactobacillus strains. Biotechnol Biotechnol Equip. 2014; 28:941–948.
   PubMed Web of Science ®Google Scholar
• Iliev I, Vasileva T, Bivolarski V, et al. Metabolic profiling of xylooligosaccharides by lactobacilli. MDPI Polymers. 2020;12(10):2387.
   PubMed Web of Science ®Google Scholar
• Vasquez A, Forsgren E, Fries I, et al. Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One. 2012;7(3):e33188.
   PubMed Web of Science ®Google Scholar
• Asenjo F, Olmos A, Henriquez-Piskulich P, et al. Genome sequencing and analysis of the first complete genome of Lactobacillus kunkeei strain MP2, an Apis mellifera gut isolate. Peer J. 2016; 4:e1950.
   PubMed Web of Science ®Google Scholar
• Passerini D, Vuillemin M, Ufarte L, et al. Inventory of the GH70 enzymes encoded by Leuconostoc citreum NRRL B-1299 - identification of three novel α-transglucosylases. Febs J. 2015;282(11):2115–2130.
   PubMed Web of Science ®Google Scholar
• Bozonnet S, Dols-Laffargue M, Fabre E, et al. Molecular characterization of DSR-E, an alpha-1,2 linkage-synthesizing dextransucrase with two catalytic domains. J Bacteriol. 2002;184(20):5753–5761.
   PubMed Web of Science ®Google Scholar
• Claverie M, Cioci G, Vuillemin M, et al. Investigation of the determinants responsible for low molar mass dextran formation by DSR-M dextransucrase. ACS Catal. 2017;7(10):7106–7119.
   Web of Science ®Google Scholar
• Remaud-Simeon M, Willemot R-M, Sarcabal P, et al. Glucansucrases: molecular engineering and oligosaccharide synthesis. J Mol Catal B Enzym. 2000;10(1-3):117–128.
   Google Scholar
• Manning TS, Gibson GR. Prebiotics. Best Pract Res Cl Ga. 2004;18(2):287–298.
   Web of Science ®Google Scholar
• Koepsell HJ, Tsuchiya HM, Hellman NN, et al. Enzymatic synthesis of dextran; acceptor specificity and chain initiation. J Biol Chem. 1953;200(2):793–801.
   PubMed Web of Science ®Google Scholar
• Robyt JF, Eklund SH. Relative quantitative effects of acceptors in the reaction of Leuconostoc mesenteroides B-512F dextransucrase. Carbohydr Res. 1983; 121:279–286.
   PubMed Web of Science ®Google Scholar
• Cote GL, Holt SM, Miller-Formore C. Prebiotic oligosaccharides via alternansucrase acceptor reactions. In: Eggleston G, Cote GL, editors. Oligosaccharides in Food and Agriculture, ACS Symposium Series. Washington, DC: Oxford University Press, 2003. Vol 849, p. 76–89.
   Google Scholar
• Cote GL, Robyt JF. Acceptor reactions of alternansucrase from Leuconostoc mesenteroides NRRL B-1355. Carbohydr Res. 1982; 111:127–142.
   Web of Science ®Google Scholar
• Leathers TD, Ahlgren JA, Cote GL. Alternansucrase mutants of L. mesenteroides strain NRRL B-21138. J Ind Microbiol Biot. 1997;18(4):278–283.
   Web of Science ®Google Scholar
• van den Broek LAM, Hinz SWA, Beldman G, et al. Bifidobacterium carbohydrases-their role in breakdown and synthesis of (potential) prebiotics. Mol Nutr Food Res. 2008;52(1):146–163.
   PubMed Web of Science ®Google Scholar
• Ganzle MG, Follador R. Metabolism of oligosaccharides and starch in lactobacilli: a review. Front Microbiol. 2012; 3:1–15.
   PubMed Web of Science ®Google Scholar
• de Vos WM, Vaughan EE. Genetics of lactose utilization in lactic acid bacteria. FEMS Microbiol Rev. 1994;15(2-3):217–237.
   PubMed Web of Science ®Google Scholar
• Barrangou R, Altermann E, Hutkins R, et al. Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus. Proc Natl Acad Sci U S A. 2003;100(15):8957–8962.
   PubMed Web of Science ®Google Scholar
• Makarova K, Slesarev A, Wolf Y, et al. Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A. 2006;103(42):15611–15616.
   PubMed Web of Science ®Google Scholar
• Siezen RJ, van Hylckama Vlieg JE. Genomic diversity and versatility of Lactobacillus plantarum, a natural metabolic engineer. Microb Cell Fact. 2011; 10(Suppl. 1):S3.
   PubMedGoogle Scholar
• Neubauer H, Glaasker E, Hammes WP, et al. Mechanism of maltose uptake and glucose excretion in Lactobacillus sanfrancisco. J Bacteriol. 1994;176(10):3007–3012.
   PubMed Web of Science ®Google Scholar
• Moller MS, Fredslund F, Nakai H, et al. Enzymology and structure of the GH13_31 glucan 1,6-α-glucosidase that confers isomaltooligosaccharide utilization in the probiotic Lactobacillus acidophilus NCFM. J Bacteriol. 2012;194(16):4249–4259.
   PubMed Web of Science ®Google Scholar
• Sanz ML, Cote GL, Gibson GR, et al. Prebiotic properties of alternansucrase maltose-acceptor oligosaccharides. J Agric Food Chem. 2005;53(15):5911–5916.
   PubMed Web of Science ®Google Scholar
• Sanz ML, Cote GL, Gibson GR, et al. Influence of glycosidic linkages and molecular weight on the fermentation of maltose-based oligosaccharides by human gut bacteria. J Agric Food Chem. 2006;54(26):9779–9784.
   PubMed Web of Science ®Google Scholar