Efficient biocatalytic synthesis of D-tagatose 1,6-diphosphate by LacC-catalysed phosphorylation of D-tagatose 6-phosphate

References

• Abranches J, Chen YYM, Burne RA. 2004. Galactose metabolism by Streptococcus mutans. Appl Environ Microbiol. 70:6047–6052.
   PubMed Web of Science ®Google Scholar
• Anderson RL, Wenger WC, Bissett DL. 1982. D-Galactose 6-phosphate and D-tagatose 6-phosphate. Methods Enzymol. 89:93–98.
   Web of Science ®Google Scholar
• Bissett DL, Anderson RL. 1974. Lactose and D-galactose metabolism in Group N Streptococci: presence of enzymes for both the D-galactose 1-phosphate and d-tagatose 6-phosphate pathways. J Bacteriol. 117:318–320.
   PubMed Web of Science ®Google Scholar
• Bissett DL, Anderson RL. 1980a. Lactose and D-galactose metabolism in Staphylococcus aureus. 111. Purification and properties of d-tagatose-6-phosphate kinase. J Biol Chem. 255:8745–8749.
   PubMed Web of Science ®Google Scholar
• Bissett DL, Anderson RL. 1980b. D-tagatose-6-phosphate kinase from Staphylococcus aureus. Methods Enzymol. 90:87–91.
   Web of Science ®Google Scholar
• Bissett DL, Wenger WC, Anderson RL. 1980. Lactose and D-galactose metabolism in Staphylococcus aureus. II. Isomerization of D-galactose 6-phosphate to D-tagatose 6-phosphate by a specific D-galactose-6-phosphate isomerase. J Biol Chem. 255:8740–8744.
   PubMed Web of Science ®Google Scholar
• Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248–254.
   PubMed Web of Science ®Google Scholar
• Crans DC, Kazlauskas RJ, Hirschbein BL, Wong CH, Abril O, Whitesides GM. 1987. Enzymatic regeneration of adenosine 5′-triphosphate: acetyl phosphate, phosphoenol-pyruvate, methoxycarbonyl phosphate, dihydroxyacetone phosphate, 5-phospho-α-D-ribosyl pyrophosphate, uridine-5′-diphosphoglucose. Vol. 136. In: Methods in enzymology. Academic Press; p. 263–280.
   Google Scholar
• Ehrlich F, Guttmann R. 1934. Zur Kenntnis der d‐Galakturonsäure, II. Mitteil.: Ihre Umlagerung in 5‐Keto‐l‐galaktonsäure. Ber. 67:573–589.
   Google Scholar
• Eyrisch O, Sinerius G, Fessner WD. 1993. Facile enzymic de novo synthesis and NMR spectroscopic characterization of d-tagatose 1,6-bisphosphate. Carbohydrate Res. 238:287–306.
   Web of Science ®Google Scholar
• Fessner WD, Badía J, Eyrisch O, Schneider A, Sinerius G. 1992. Enzymatic syntheses of rare ketose 1-phosphates. Tetrahedron Lett. 33:5231–5234.
   Web of Science ®Google Scholar
• Fessner WD, Eyrisch O. 1992. One‐pot synthesis of tagatose 1, 6‐bisphosphate by diastereoselective enzymatic aldol addition. Angew Chem Int Ed Engl. 31:56–58.
   Web of Science ®Google Scholar
• Gauss D, Sánchez‐Moreno I, Oroz‐Guinea I, García‐Junceda E, Wohlgemuth R. 2018. Phosphorylation catalyzed by dihydroxyacetone kinase. Eur J Org Chem. 2018:2892–2895.
   Google Scholar
• Gauss D, Schoenenberger B, Molla GS, Kinfu BM, Chow J, Liese A, Streit W, Wohlgemuth R. 2016. Biocatalytic phosphorylation of metabolites. In: Liese A, Hilterhaus L, Kettling U, Antranikian G, editors. Applied biocatalysis – from fundamental science to industrial applications. Weinheim, Germany: Wiley-VCH; p.147–177.
   Google Scholar
• Gauss D, Schoenenberger B, Wohlgemuth R. 2014. Chemical and enzymatic methodologies for the synthesis of enantiomerically pure glyceraldehyde 3-phosphates. Carbohydrate Res. 389:18–24.
   PubMed Web of Science ®Google Scholar
• Hamilton IR, Lebtag H. 1979. Lactose metabolism by Streptococcus mutans: evidence for induction of the tagatose 6-phosphate pathway. J Bacteriol. 140:1102–1104.
   PubMed Web of Science ®Google Scholar
• Hardt N, Kind S, Schoenenberger B, Eggert T, Obkircher M, Wohlgemuth R. 2019. Facile synthesis of D-xylulose-5-phosphate and L-xylulose-5-phosphate by xylulokinase-catalyzed phosphorylation. Biocatal Biotransform. doi:10.1080/10242422.2019.1630385
   Web of Science ®Google Scholar
• Hardt N, Kinfu BM, Chow J, Streit WR, Schoenenberger B, Obkircher M, Wohlgemuth R. 2017. Biocatalytic asymmetric phosphorylation catalyzed by recombinant glycerate-2-kinase. ChemBioChem 18:1518–1522.
   PubMed Web of Science ®Google Scholar
• Heidlas JE, Lees WJ, Whitesides GM. 1992. Practical enzyme-based syntheses of uridine 5'-diphosphogalactose and uridine 5'-diphospho-N-acetylgalactosamine on a gram scale. J Org Chem. 57:152–157.
   Web of Science ®Google Scholar
• Hélaine V, Mahdi R, Sudhir Babu GV, de Berardinis V, Wohlgemuth R, Lemaire M, Guérard ‐, Hélaine C. 2015. Straightforward synthesis of terminally phosphorylated L‐sugars via multienzymatic cascade reactions. Adv Synth Catal. 357:1703–1708.
   Web of Science ®Google Scholar
• Hoffmeister D, Yang J, Liu L, Thorson JS. 2003. Creation of the first anomeric D/L-sugar kinase by means of directed evolution. Proc Natl Acad Sci USA. 100:13184–13189.
   PubMed Web of Science ®Google Scholar
• Huang K, Parmeggiani F, Pallister E, Huang CJ, Liu FF, Li Q, Birmingham WR, Both P, Thomas B, Liu L, et al. 2018. Characterisation of a bacterial galactokinase with high activity and broad substrate tolerance for chemoenzymatic synthesis of 6‐aminogalactose‐1‐phosphate and analogues. ChemBioChem 19:388–394.
   PubMed Web of Science ®Google Scholar
• Izumori K. 2006. Izumoring: a strategy for bioproduction of all hexoses. J Biotechnol. 124:717–722.
   PubMed Web of Science ®Google Scholar
• Jayamuthunagai J, Gautam P, Srisowmeya G, Chakravarthy M. 2017. Biocatalytic production of D-tagatose: a potential rare sugar with versatile applications. Crit Rev Food Sci Nutr. 57:3430–3437.
   PubMed Web of Science ®Google Scholar
• Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680–685.
   PubMed Web of Science ®Google Scholar
• Lengeler JW. 2015. PTS 50: past, present and future, or diauxie revisited. J Mol Microbiol Biotechnol. 25:79–93.
   PubMed Web of Science ®Google Scholar
• Liu Y, Nishimoto M, Kitaoka M. 2015. Facile enzymatic synthesis of sugar 1-phosphates as substrates for phosphorylases using anomeric kinases. Carbohydr Res. 401:1–4.
   PubMed Web of Science ®Google Scholar
• Loughman JA, Caparon MG. 2006. A novel adaptation of aldolase regulates virulence in Streptococcus pyogenes. Embo J. 25:5414–5422.
   PubMed Web of Science ®Google Scholar
• Matsumi R, Hellriegel C, Schoenenberger B, Milesi T, Van Der Oost J, Wohlgemuth R. 2014. Biocatalytic asymmetric phosphorylation of mevalonate. RSC Adv. 4:12989–12994.
   Web of Science ®Google Scholar
• Miallau L, Hunter WN, McSweeney SM, Leonard GA. 2007. Structures of Staphylococcus aureus D-tagatose-6-phosphate kinase implicate domain motions in specificity and mechanism. J Biol Chem. 282:19948–19957.
   PubMed Web of Science ®Google Scholar
• Moye ZD, Zeng L, Burne RA. 2014. Fueling the caries process: carbohydrate metabolism and gene regulation by Streptococcus mutans. J Oral Microbiol. 6:24878.
   Web of Science ®Google Scholar
• Nobelmann B, Lengeler JW. 1996. Molecular analysis of the gat genes from Escherichia coli and of their roles in galactitol transport and metabolism. J Bacteriol. 178:6790–6795.
   PubMed Web of Science ®Google Scholar
• Nolle N, Felsl A, Heermann R, Fuchs TM. 2017. Genetic characterization of the galactitol utilization pathway of Salmonella enterica serovar Typhimurium. J Bacteriol. 199:e00595–16.
   PubMed Web of Science ®Google Scholar
• Oh DK. 2007. Tagatose: properties, applications, and biotechnological processes. Appl Microbiol Biotechnol. 76:1–8.
   PubMed Web of Science ®Google Scholar
• Postma PW, Lengeler JW, Jacobson GR. 1993. Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev. 57:543–594.
   PubMedGoogle Scholar
• Rios-Mercadillo, V M, Whitesides, G M. 1979. Enzymic synthesis of sn-glycerol 3-phosphate. J Am Chem Soc.101:5828–5829.
   Web of Science ®Google Scholar
• Rosey EL, Oskouian B, Stewart GC. 1991. Lactose metabolism by Staphylococcus aureus: characterization of lacABCD, the structural genes of the tagatose 6-phosphate pathway. J Bacteriol. 173:5992–5998.
   PubMed Web of Science ®Google Scholar
• Rosey EL, Stewart GC. 1992. Nucleotide and deduced amino acid sequences of the lacR, lacABCD, and lacFE genes encoding the repressor, tagatose 6-phosphate gene cluster, and sugar-specific phosphotransferase system components of the lactose operon of Streptococcus mutans. J Bacteriol. 174:6159–6170.
   PubMed Web of Science ®Google Scholar
• Saier MH. Jr 2015. The Bacterial Phosphotransferase System: new frontiers 50 years after its discovery. J Mol Microbiol Biotechnol. 25:73–78.
   PubMed Web of Science ®Google Scholar
• Sha F, Zheng Y, Chen J, Chen K, Cao F, Yan M, Ouyang P. 2018. D-Tagatose manufacture through bio-oxidation of galactitol derived from waste xylose mother liquor. Green Chem. 20:2382–2391.
   Web of Science ®Google Scholar
• Shakeri-Garakani A, Brinkkötter A, Schmid K, Turgut S, Lengeler JW. 2004. The genes and enzymes for the catabolism of galactitol, D-tagatose, and related carbohydrates in Klebsiella oxytoca M5a1 and other enteric bacteria display convergent evolution. Mol Gen Genomics 271:717–728.
   PubMed Web of Science ®Google Scholar
• Studier FW, Moffatt BA. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol. 189:113–130.
   PubMed Web of Science ®Google Scholar
• Thomas TD. 1975. Tagatose-1, 6-diphosphate activation of lactate dehydrogenase from Streptococcus cremoris. Biochem Biophys Res Commun. 63:1035–1047.
   PubMed Web of Science ®Google Scholar
• Thompson J. 1987. Regulation of sugar transport and metabolism in lactic acid bacteria. FEMS Microbiol Rev. 46:221–231.
   Google Scholar
• Totton EL, Lardy HA. 1957. Synthetic ketohexose phosphates: I. D-tagatose-6-phosphate. Methods Enzymol. 3:174–176.
   Web of Science ®Google Scholar
• Tung TC, Ling KH, Byrne WL, Lardy HA. 1954. Substrate specificity of muscle aldolase. Biochim Biophys Acta. 14:488–494.
   PubMedGoogle Scholar
• Van der Heiden E, Delmarcelle M, Lebrun S, Freichels R, Brans A, Vastenavond CM, Galleni M, Joris B. 2013. A pathway closely related to the (D)-tagatose pathway of gram-negative enterobacteria identified in the gram-positive bacterium Bacillus licheniformis. Appl Environ Microbiol. 79:3511–3515.
   PubMed Web of Science ®Google Scholar
• Van der Heiden E, Delmarcelle M, Simon P, Counson M, Galleni M, Freedberg DI, Thompson J, Joris B, Battistel MD. 2015. Synthesis and physicochemical characterization of d-tagatose-1-phosphate: the substrate of the tagatose-1-phosphate kinase in the phosphotransferase system-mediated d-tagatose catabolic pathway of Bacillus licheniformis. J Mol Microbiol Biotechnol. 25:106–119.
   PubMed Web of Science ®Google Scholar
• van Rooijen RJ, van Schalkwijk S, de Vos WM. 1991. Molecular cloning, characterization, and nucleotide sequence of the tagatose 6-phosphate pathway gene cluster of the lactose operon of Lactococcus lactis. J Biol Chem. 266:7176–7181.
   PubMed Web of Science ®Google Scholar
• Wen L, Huang K, Liu Y, Wang PG. 2016. Facile enzymatic synthesis of phosphorylated ketopentoses. ACS Catal. 6:1649–1654.
   Web of Science ®Google Scholar
• Wen L, Huang K, Wei M, Meisner J, Liu Y, Garner K, Zang L, Wang X, Li X, Fang J, et al. 2015. Facile enzymatic synthesis of ketoses. Angew Chem Int Ed Engl. 54:12654–12658.
   PubMed Web of Science ®Google Scholar
• Wen L, Huang K, Zheng Y, Fang J, Kondengaden SM, Wang PG. 2016. Two-step enzymatic synthesis of 6-deoxy-L-psicose. Tetrahedron Lett. 57:3819–3822.
   PubMed Web of Science ®Google Scholar
• Wen L, Zang L, Huang K, Li S, Wang R, Wang PG. 2016. Efficient enzymatic synthesis of L-rhamnulose and L-fuculose. Bioorg Med Chem Lett. 26:969–972.
   PubMed Web of Science ®Google Scholar
• Wichelecki DJ, Vetting MW, Chou L, Al-Obaidi N, Bouvier JT, Almo SC, Gerlt JA. 2015. ATP-binding cassette (ABC) transport system solute-binding protein-guided identification of novel d-altritol and galactitol catabolic pathways in Agrobacterium tumefaciens C58. J Biol Chem. 290:28963–28976.
   PubMed Web of Science ®Google Scholar
• Wildberger P, Pfeiffer M, Brecker L, Nidetzky B. 2015. Diastereoselective synthesis of glycosyl phosphates by using a phosphorylase–phosphatase combination catalyst. Angew Chem Int Ed. 54:15867–15871.
   PubMed Web of Science ®Google Scholar
• Wohlgemuth R, Liese A, Streit W. 2017. Biocatalytic phosphorylations of metabolites: past, present, and future. Trends Biotechnol. 35:452–465.
   PubMed Web of Science ®Google Scholar
• Xu Z, Li S, Feng X, Liang J, Xu H. 2014. L-Arabinose isomerase and its use for bio-technological production of rare sugars. Appl Microbiol Biotechnol. 98:8869–8878.
   PubMed Web of Science ®Google Scholar
• Yang J, Fu X, Jia Q, Shen J, Biggins JB, Jiang J, Zhao J, Schmidt JJ, Wang PG, Thorson JS. 2003. Studies on the substrate specificity of Escherichia coli galactokinase. Org Lett. 5:2223–2226.
   PubMed Web of Science ®Google Scholar
• Zhang W, Zhang T, Jiang B, Mu W. 2017. Enzymatic approaches to rare sugar production. Biotechnol Adv. 35:267–274.
   PubMed Web of Science ®Google Scholar
• Zhu J-S, Stiers KM, Winter SM, Garcia AD, Versini AF, Beamer LJ, Jakeman DL. 2019. Synthesis, derivatization, and structural analysis of phosphorylated mono-, di -, and trifluorinated D-gluco-heptuloses by glucokinase: tunable phosphoglucomutase inhibition. ACS Omega. 4:7029–7037.
   PubMed Web of Science ®Google Scholar