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4.A.3 The PTS Lactose-N,N'-Diacetylchitobiose-β-glucoside (Lac) Family

The Lac family includes several sequenced lactose (β-galactoside) porters of Gram-positive bacteria as well as the E. coli and Borrelia burgdorferi N,N'-diacetylchitobiose (Chb) porters. The former can transport aromatic β-glucosides and cellobiose as well as the chitin disaccharide, Chb. However, only Chb induces expression of the chb operon. While the Lac porters consist of two polypeptide chains (IIA and IICB), the Chb porters of E. coli and B. burgdorferi consist of three (IIA, IIB and IIC). In E. coli, the IIAChb protein has been shown to form a stable dimer both when phosphorylated and when unphosphorylated.  The IIC domains of these permeases are believed to have a uniform topology with 10 TMSs (Cao et al. 2011; Vastermark and Saier 2016).

In E. coli, the IIBChb is a monomer. Two IIBChb monomers associate with the IIAChb dimer. The structure of the IIB domain of the Chb porter has been determined both by NMR and by x-ray crystallography. It exhibits an α/β doubly wound superfold. This is different from the structure of the IIBGlc and IIBMan domains. IIBSgc, believed to function in pentose transport, is homologous to IIBLac and IIBChb. In B. subtilis, a PTS porter similar to the Chb porter of E. coli is believed to transport lichenan (a β-1,3;1,4 glucan) degradation products, oligosaccharides of 2-4 glucose units. The B. burgdorferi system is more similar to the Bacillus Lic system than the E. coli Chb system. The IIC domains of members of the Lac family are all more similar to each other than they are to those of the Glc, Bgl, Fru and Mtl families.

This family belongs to the: PTS-GFL Superfamily.

References associated with 4.A.3 family:

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Cao, T.N., P. Joyet, F.M.D. Aké, E. Milohanic, and J. Deutscher. (2019). Studies of the Listeria monocytogenes Cellobiose Transport Components and Their Impact on Virulence Gene Repression. J. Mol. Microbiol. Biotechnol. 29: 10-26. 31269503
Cao, Y., X. Jin, E.J. Levin, H. Huang, Y. Zong, M. Quick, J. Weng, Y. Pan, J. Love, M. Punta, B. Rost, W.A. Hendrickson, J.A. Javitch, K.R. Rajashankar, and M. Zhou. (2011). Crystal structure of a phosphorylation-coupled saccharide transporter. Nature 473: 50-54. 21471968
Francl, A.L., J.L. Hoeflinger, and M.J. Miller. (2012). Identification of lactose phosphotransferase systems in Lactobacillus gasseri ATCC 33323 required for lactose utilization. Microbiology 158: 944-952. 22282520
Hall, B.G., K. Imai, and C.P. Romano. (1982). Genetics of the lac-PTS system of Klebsiella. Genet Res 39: 287-302. 7117837
Imai, K. and B.G. Hall. (1981). Properties of the lactose transport system in Klebsiella sp. strain CT-1. J. Bacteriol. 145: 1459-1462. 6907272
Kachroo, A.H., A.K. Kancherla, N.S. Singh, U. Varshney, and S. Mahadevan. (2007). Mutations that alter the regulation of the chb operon of Escherichia coli allow utilization of cellobiose. Mol. Microbiol. 66(6):1382-1395. 18028317
Keyhani, N.O. and S. Roseman. (1997). Wild-type Escherichia coli grows on the chitin disaccharide N,N'-diacetylchitobiose, by expressing the cel operon. Proc. Natl. Acad. Sci. USA 94: 14367-14371. 9405618
Keyhani, N.O., K. Bacia, and S. Roseman. (2000). The transport/phosphorylation of N,N'-diacetylchitobiose in Escherichia coli. J. Biol. Chem. 275: 33102-33109. 10913119
Keyhani, N.O., L.X. Wang, Y.C. Lee, and S. Roseman. (2000). The chitin disaccharide, N,N'-diacetylchitobiose, is catabolized by Escherichia coli and is transported/phosphorylated by the phosphoenolpyruvate: glycose phosphotransferase system. J. Biol. Chem. 275: 33084-33090. 10913117
Keyhani, N.O., M.E. Rodgers, B. Demeler, J.C. Hansen, and S. Roseman. (2000). Analytical sedimentation of the IIAChb and IIBChb proteins of the Escherichia coli N,N'-diacetylchitobiose phosphotransferase system. J. Biol. Chem. 275: 33110-33115. 10913122
Keyhani, N.O., O. Boudker, and S. Roseman. (2000). Isolation and characterization of IIAChb, a soluble protein of the enzyme II complex required for the transport/phosphorylation of N,N'-diacetylchitobiose in Escherichia coli. J. Biol. Chem. 275: 33091-33101. 10913118
Kowalczyk, M., M. Cocaign-Bousquet, P. Loubiere, and J. Bardowski. (2008). Identification and functional characterisation of cellobiose and lactose transport systems in Lactococcus lactis IL1403. Arch. Microbiol. 189(3): 187-196. 17909747
Kowolik, C.M. and W. Hengstenberg. (1998). The lactose transporter of Staphylococcus aureus--overexpression, purification and characterization of the histidine-tagged domains IIC and IIB. Eur J Biochem 257: 389-394. 9826184
Meibom, K.L., X.B. Li, A.T. Nielsen, C.Y. Wu, S. Roseman, and G.K. Schoolnik. (2004). The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. USA 101: 2524-2529. 14983042
Nguyen, T.X., M.R. Yen, R.D. Barabote, and M.H. Saier, Jr. (2006). Topological predictions for integral membrane permeases of the phosphoenolpyruvate:sugar phosphotransferase system. J. Mol. Microbiol. Biotechnol. 11: 345-360. 17114898
Reizer, J., A. Charbit, A. Reizer, and M.H. Saier, Jr. (1996). Novel phosphotransferase system genes revealed by bacterial genome analysis: Operons encoding homologues of sugar-specific permease domains of the phosphotransferase system and pentose catabolic enzymes. Genome Sci. Technol. 1: 53-75.
Reizer, J., S. Bachem, A. Reizer, M. Arnaud, M.H. Saier, Jr., and J. Stülke. (1999). Novel phosphotransferase system genes revealed by genome analysis – the complete complement of PTS proteins encoded within the genome of Bacillus subtilis. Microbiology 145: 3419-3429. 10627040
Rosey, E.L. and G.C. Stewart. (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. 1400164
Sadaie, Y., H. Nakadate, R. Fukui, L.M. Yee, and K. Asai. (2008). Glucomannan utilization operon of Bacillus subtilis. FEMS Microbiol. Lett. 279: 103-109. 18177310
Tilly, K., A.F. Elias, J. Errett, E. Fischer, R. Iyer, I. Schwartz, J.L. Bono, and P. Rosa. (2001). Genetics and regulation of chitobiose utilization in Borrelia burgdorferi. J. Bacteriol. 183: 5544-5553. 11544216
Tobisch, S., P. Glaser, S. Krüger, and M. Hecker. (1997). Identification and characterization of a new β-glucoside utilization system in Bacillus subtilis. J. Bacteriol. 179: 496-506. 8990303
Toratani, T., T. Shoji, T. Ikehara, K. Suzuki, and T. Watanabe. (2008). The importance of chitobiase and N-acetylglucosamine (GlcNAc) uptake in N,N'-diacetylchitobiose [(GlcNAc)2] utilization by Serratia marcescens 2,170. Microbiology 154: 1326-1332. 18451041
Van Montfort, R.L.M., T. Pijning, K.H. Kalk, J. Reizer, M.H. Saier, Jr., M.M.G.M. Thunnissen, G.T. Robillard, and B.W. Dijkstra. (1997). The structure of an energy-coupling protein from bacteria, IIBcellobiose, reveals similarity to eukaryotic protein tyrosine phosphatases. Structure 5: 217-225. 9032081
Vastermark, A. and M.H. Saier, Jr. (2016). Time to Stop Holding the Elevator: A New Piece of the Transport Protein Mechanism Puzzle. Structure 24: 845-846. 27276425
Wu, M.C., Y.C. Chen, T.L. Lin, P.F. Hsieh, and J.T. Wang. (2012). Cellobiose-specific phosphotransferase system of Klebsiella pneumoniae and its importance in biofilm formation and virulence. Infect. Immun. 80: 2464-2472. 22566508