How Phosphotransferase System-Related Protein Phosphorylation Regulates Carbohydrate Metabolism in Bacteria
Tóm tắt
The phosphoenolpyruvate(PEP):carbohydrate phosphotransferase system (PTS) is found only in bacteria, where it catalyzes the transport and phosphorylation of numerous monosaccharides, disaccharides, amino sugars, polyols, and other sugar derivatives. To carry out its catalytic function in sugar transport and phosphorylation, the PTS uses PEP as an energy source and phosphoryl donor. The phosphoryl group of PEP is usually transferred via four distinct proteins (domains) to the transported sugar bound to the respective membrane component(s) (EIIC and EIID) of the PTS. The organization of the PTS as a four-step phosphoryl transfer system, in which all P derivatives exhibit similar energy (phosphorylation occurs at histidyl or cysteyl residues), is surprising, as a single protein (or domain) coupling energy transfer and sugar phosphorylation would be sufficient for PTS function. A possible explanation for the complexity of the PTS was provided by the discovery that the PTS also carries out numerous regulatory functions. Depending on their phosphorylation state, the four proteins (domains) forming the PTS phosphorylation cascade (EI, HPr, EIIA, and EIIB) can phosphorylate or interact with numerous non-PTS proteins and thereby regulate their activity. In addition, in certain bacteria, one of the PTS components (HPr) is phosphorylated by ATP at a seryl residue, which increases the complexity of PTS-mediated regulation. In this review, we try to summarize the known protein phosphorylation-related regulatory functions of the PTS. As we shall see, the PTS regulation network not only controls carbohydrate uptake and metabolism but also interferes with the utilization of nitrogen and phosphorus and the virulence of certain pathogens.
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Adhya, S. 1996. The lac and gal operons today, p. 181-200. In E. C. C. Lin and A. S. Lynch (ed.), Regulation of gene expression in Escherichia coli. R.G. Landes Company, Austin, Tex.
J. Mol. Microbiol. Biotechnol.
Boos, W., and J. M. Lucht. 1996. Periplasmic binding protein-dependent ABC transporters, p. 1175-1209. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C.
Bramley, H. F., and H. L. Kornberg. 1987. Nucleotide sequence of bglC, the gene specifying enzyme IIbgl of the PEP:sugar phosphotransferase system in Escherichia coli K12, and overexpression of the gene product. J. Gen. Microbiol.133:563-573.
Busby, S., and A. Kolb. 1996. The CAP modulon, p. 255-279. In E. C. C. Lin and A. S. Lynch (ed.), Regulation of gene expression in Escherichia coli. R. G. Landes Company, Austin, Tex.
Christiansen, I., and W. Hengstenberg. 1996. Cloning and sequencing of two genes from Staphylococcus carnosus coding for glucose-specific PTS and their expression in Escherichia coli K-12. Mol. Gen. Genet.250:375-379.
Contesse, G., M. Crépin, F. Gros, A. Ullmann, and J. Monod. 1969. On the mechanism of catabolite repression, p. 401-415. In J. R. Beckwith and D. Zipser (ed.), The lactose operon. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
Darbon, E., A. Galinier, D. Le Coq, and J. Deutscher. 2001. Phosphotransfer functions of mutated Bacillus subtilis HPr-like protein Crh carrying a histidine in the active site. J. Mol. Microbiol. Biotechnol.3:439-444.
Deutscher, J., A. Galinier, and I. Martin-Verstraete. 2002. Carbohydrate uptake and metabolism, p. 129-150. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, D.C.
Dienert, F. 1900. Sur la fermentation du galactose et sur l'accoutumence des levures à ce sucre. Ann. Pasteur.14:139-189.
Eppler, T., and W. Boos. 1999. Glycerol-3-phosphate-mediated repression of malT in Escherichia coli does not require metabolism, depends on enzyme IIAGlc and is mediated by cAMP levels. Mol. Microbiol.33:1221-1231.
Esquinas-Rychen, M., and B. Erni. 2001. Facilitation of bacteriophage lambda DNA injection by inner membrane proteins of the bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system (PTS). J. Mol. Microbiol. Biotechnol.3:361-370.
Fabret C. 1996. Projet génome Bacillus subtilis: séquençage et analyse de la région chromosomique entre les loci cysB et hisA. Ph.D. thesis. Université de la Mediterranée Aix-Marseille Marseille France.
Faires, N., S. Tobisch, S. Bachem, I. Martin-Verstraete, M. Hecker, and J. Stülke. 1999. The catabolite control protein CcpA controls ammonium assimilation in Bacillus subtilis. J. Mol. Microbiol. Biotechnol.1:141-148.
Gay P. 1979. The vectorial metabolism of carbohydrates and the catabolism of fructose in Bacillus subtilis Marburg: genetic and biochemical studies. Ph.D. thesis. University of Paris VI Paris France.
Gershanovitch, V. N., T. N. Bolshakova, M. L. Molchanova, A. M. Umyarov, O. Y. Dobrynina, Y. A. Grigorenko, and R. S. Erlagaeva. 1989. Fructose-specific phosphoenolpyruvate dependent phosphotransferase system of Escherichia coli: its alterations and adenylate cyclase activity. FEMS Microbiol. Rev.63:125-134.
Gutknecht, R., R. Beutler, L. F. Garcia-Alles, U. Baumann, and B. Erni. 2001. The dihydroxyacetone kinase of Escherichia coli utilizes a phosphoprotein instead of ATP as phosphoryl donor. EMBO J.15:2480-2486.
Halbedel, S., C. Hames, and J. Stülke. 2007. Regulation of carbon metabolism in the mollicutes and its relation to virulence. J. Mol. Microbiol. Biotechnol.12:145-152.
Hanamura, A., and H. Aiba. 1992. A new aspect of transcriptional control of the Escherichia coli crp gene: positive autoregulation. Mol. Microbiol.6:2489-2497.
Hogema, B. M., J. C. Arents, R. Bader, K. Eijkemans, T. Inada, H. Aiba, and P. W. Postma. 1998. Inducer exclusion by glucose 6-phosphate in Escherichia coli. Mol. Microbiol.28:755-765.
Jacobson, G. R., and C. Saraceni-Richards. 1993. The Escherichia coli mannitol permease as a model for transport via the bacterial phosphotransferase system. J. Bioenerg. Biomembr.25:621-626.
Jin, R. Z., and E. C. C. Lin. 1984. An inducible phosphoenolpyruvate:dihydroxyacetone phosphotransferase system in Escherichia coli. J. Gen. Microbiol.130:83-88.
Jones-Mortimer, M. C., and H. L. Kornberg. 1980. Amino-sugar transport systems of Escherichia coli K12. J. Gen. Microbiol.117:369-376.
Koehler, T. M. 2002. Bacillus anthracis genetics and virulence gene regulation. Curr. Top. Microbiol. Immunol.271:143-164.
Koo, B. M., and Y.-J. Seok. 2001. Regulation of glycogen concentration by the histidine-containing phosphocarrier protein HPr in Escherichia coli. J. Microbiol.39:24-30.
Kuroda, M., T. H. Wilson, and T. Tsuchiya. 2001. Regulation of galactoside transport by the PTS. J. Mol. Microbiol. Biotechnol.3:381-384.
Lengeler, J. W. 2000. Metabolic networks: a signal-oriented approach to cellular models. Biol. Chem.381:911-920.
Lin, E. C. C. 1996. Dissimilatory pathways for sugars, polyols, and carboxylates, p. 307-342. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C.
Reference deleted.
MacNab, R. M. 1996. Flagella and motility, p. 123-145. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C.
Magasanik, B. 1970. Glucose effects: inducer exclusion and repression, p. 189-219. In J. R. Beckwith and D. Zipser (ed.), The lactose operon. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
Appl. Environ. Microbiol.
Merrick, M. J., M. Taylor, M. H. Saier, Jr., and J. Reizer. 1995. The role of genes downstream of the σN structural gene rpoN in Klebsiella pneumoniae, p. 189-194. In I. A. Tikhonovitch, N. A. Provorov, V. I. Romanov, and W. E. Newton (ed.), Nitrogen fixation: fundamentals and applications. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Monedero, V., A. Mazé, G. Boël, M. Zúñiga, S. Beaufils, A. Hartke, and J. Deutscher. 2007. The phosphotransferase system of Lactobacillus casei: regulation of carbon metabolism and connection to cold shock response. J. Mol. Microbiol. Biotechnol.12:18-30.
Monod J. 1942. Recherches sur la croissance des cultures bactériennes. Hermann et Cie Paris France.
Morel, F., M. Lamarque, I. Bissardon, D. Atlan, and A. Galinier. 2001. Autoregulation of the biosynthesis of the CcpA-like protein, PepR1, in Lactobacillus delbrueckii subsp. bulgaricus. J. Mol. Microbiol. Biotechnol.3:63-66.
Muramatsu, S., and T. Mizuno. 1989. Nucleotide sequence of the region encompassing the glpKF operon and its upstream region containing a bent DNA sequence of Escherichia coli. Nucleic Acids Res.17:4378.
Neidhardt, F. C., and M. A. Savageau. 1996. Regulation beyond the operon, p. 1310-1324. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C.
Ninfa, A. J., P. Jiang, M. R. Atkinson, and J. A. Peliska. 2000. Integration of antagonistic signals in the regulation of nitrogen assimilation in Escherichia coli. Curr. Top. Cell. Regul.36:31-75.
Parche, S., A. W. Thomae, M. Schlicht, and F. Titgemeyer. 2001. Corynebacterium diphtheriae: a PTS view to the genome. J. Mol. Microbiol. Biotechnol.3:415-422.
Pascal M. J. F. 1976. The enzymes of sucrose metabolism and the regulation of their synthesis in Bacillus subtilis Marburg. Ph.D. thesis. University of Paris VII Paris France.
Pecher, A., I. Rennner, and J. W. Lengeler. 1983. The phosphoenolpyruvate-dependent carbohydrate:phosphotransferase system enzyme II. A new class of chemosensors in bacterial chemotaxis, p. 517-531. In H. Sund and C. Veegher (ed.), Mobility and recognition in cell biology. Walter de Gruyter & Co., Berlin, Germany.
Penin, F., A. Favier, R. Montserret, B. Brutscher, J. Deutscher, D. Marion, and A. Galinier. 2001. Characterisation of the oligomerisation state of the Bacillus subtilis catabolite repression HPr-like protein, Crh. J. Mol. Microbiol. Biotechnol.3:429-432.
Peterkofsky, A. 1981. Escherichia coli adenylate cyclase as a sensor of sugar transport function. Adv. Cyclic Nucleotide Res.14:215-228.
Postma, P. W., C. P. Broekhuizen, A. R. J. Schuitema, A. P. Vogler, and J. W. Lengeler. 1988. Carbohydrate transport and metabolism in Escherichia coli and Salmonella typhimurium: regulation by the PEP:carbohydrate phosphotransferase system, p. 43-52. In F. Palmieri and E. Quagliariello (ed.), Molecular basis of biomembrane transport. Elsevier Science Publishers, Amsterdam, The Netherlands.
Preiss, J., and T. Romeo. 1989. Physiology, biochemistry and genetics of bacterial glycogen synthesis. Adv. Microb. Physiol.30:183-238.
Rajagopal, P., E. B. Waygood, J. Reizer, M. H. Saier, Jr., and R. E. Klevit. 1997. Demonstration of protein-protein interaction specificity by NMR chemical shift mapping. Protein Sci.6:2624-2627.
Ramos, I., S. Guzmán, L. Escalante, I. Imriskova, R. Rodríguez-Sanoja, S. Sanchez, and E. Langley. 2004. Glucose kinase alone cannot be responsible for carbon source regulation in Streptomyces peucetius var. caesius. Res. Microbiol.155:267-274.
Ramseier, T. M., J. Reizer, E. Küster, W. Hillen, and M. H. Saier, Jr. 1995. In vitro binding of the CcpA protein of Bacillus megaterium to cis-acting catabolite responsive elements (CREs) of gram-positive bacteria. FEMS Microbiol. Lett.129:207-214.
Reizer, J., I. T. Paulsen, A. Reizer, F. Titgemeyer, and M. H. Saier, Jr. 1996. Novel phosphotransferase system genes revealed by bacterial genome analysis: the complete complement of pts genes in Mycoplasma genitalium. Microb. Comp. Genomics1:151-163.
Reizer, J., and A. Peterkofsky. 1987. Regulatory mechanisms for sugar transport in gram-positive bacteria, p. 333-364. In J. Reizer and A. Peterkofsky (ed.), Sugar transport and metabolism in gram-positive bacteria. Ellis Horwood, Chichester, United Kingdom.
Rohwer, J. M., J.-H. S. Hofmeyr, and P. W. Postma. 1998. Retro-regulation of the bacterial phosphotransferase system: a kinetic model, p. 340-344. In C. Larsson, I. L. Pählman, and L. Gustafsson (ed.), BioThermoKinetics in the post genomic era. Chalmers University of Technology, Göteborg, Sweden.
Romano, A. H., and M. H. Saier, Jr. 1992. Evolution of the bacterial phosphoenolpyruvate:sugar phosphotransferase system. Section I. Physiological and organismic considerations, p. 143-170. In R. P. Mortlock (ed.), Evolution of metabolic function. CRC Press, Boca Raton, Fla.
Saier, M. H., Jr., T. M. Ramseier, and J. Reizer. 1996. Regulation of carbon utilization, p. 1325-1343. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C.
Seok, Y.-J., B. M. Koo, M. Sondej, and A. Peterkofsky. 2001. Regulation of E. coli glycogen phosphorylase activity by HPr. J. Mol. Microbiol. Biotechnol.3:385-393.
Steinhauer, K., G. S. Allen, W. Hillen, J. Stülke, and R. G. Brennan. 2002. Crystallization, preliminary X-ray analysis and biophysical characterization of HPr kinase/phosphatase of Mycoplasma pneumoniae. Acta Crystallogr.58:515-518.
Stentz, R., and M. Zagorec. 1999. Ribose utilization in Lactobacillus sakei: analysis of the regulation of the rbs operon and putative involvement of a new transporter. J. Mol. Microbiol. Biotechnol.1:165-173.
Stock, J. B., and M. G. Surette. 1996. Chemotaxis, p. 1103-1129. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C.
Tangney, M., and W. J. Mitchell. 2000. Analysis of a catabolic operon for sucrose transport and metabolism in Clostridium acetobutylicum ATCC 824. J. Mol. Microbiol. Biotechnol.2:71-80.
Taylor, B. L., and J. W. Lengeler. 1990. Transductive coupling by methylated transducing proteins and permeases of the phosphotransferase system in bacterial chemotaxis, p. 69-90. In R. C. Aloia, C. C. Curtain, and L. M. Gordon (ed.), Membrane transport and information storage. Wiley Liss, New York, N.Y.
Tchieu, J. H., V. Norris, J. S. Edwards, and M. H. Saier, Jr. 2001. The complete phosphotranferase system in Escherichia coli. J. Mol. Microbiol. Biotechnol.3:329-346.
Tian, Z. X., Q. S. Li, M. Buck, A. Kolb, and Y. P. Wang. 2001. The CRP-cAMP complex and downregulation of the glnAp2 promoter provides a novel regulatory linkage between carbon metabolism and nitrogen assimilation in Escherichia coli. Mol. Microbiol.41:911-924.
Ullmann, A., and A. Danchin. 1983. Role of cyclic AMP in bacteria. Adv. Cyclic Nucleotide Res.15:32-53.
Umbarger, H. E. 1996. Biosynthesis of the branched-chain amino acids, p. 442-457. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, D.C.
Vadeboncoeur, C., M. Frenette, and L. A. Lortie. 2000. Regulation of the pts operon in low G+C gram-positive bacteria. J. Mol. Microbiol. Biotechnol.2:483-490.
Viana, R., V. Monedero, V. Dossonnet, C. Vadeboncoeur, G. Pérez-Martínez, and J. Deutscher. 2000. Enzyme I and HPr from Lactobacillus casei: their role in sugar transport, carbon catabolite repression and inducer exclusion. Mol. Microbiol.36:570-584.
Zahler, S. A., L. G. Benjamin, B. S. Glatz, P. F. Winter, and B. J. Goldstein. 1976. Genetic mapping of the alsA, alsR, thyA, kauA, and citD markers in Bacillus subtilis, p. 35-43. In D. Schlessinger (ed.), Microbiology—1976. American Society for Microbiology, Washington, D.C.