Evidence for reciprocal evolution of the global repressor Mlc and its cognate phosphotransferase system sugar transporter.


Journal

Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692

Informations de publication

Date de publication:
01 2022
Historique:
revised: 28 08 2021
received: 03 08 2021
accepted: 02 10 2021
pubmed: 29 10 2021
medline: 18 3 2022
entrez: 28 10 2021
Statut: ppublish

Résumé

Because the bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system (PTS) is involved in the regulation of various physiological processes in addition to carbohydrate transport, its expression is precisely regulated in response to the availability of PTS sugars. The PTS consists of enzyme I and histidine phosphocarrier protein, and several sugar-specific enzymes II. In Escherichia coli, genes for enzymes II specific for glucose and related sugars are co-regulated by the global repressor Mlc, and glucose induction of the Mlc regulon genes is achieved by its interaction with glucose-specific enzyme II (EII

Identifiants

pubmed: 34708498
doi: 10.1111/1462-2920.15803
doi:

Substances chimiques

Bacterial Proteins 0
Escherichia coli Proteins 0
Mlc protein, E coli 0
Repressor Proteins 0
Phosphoenolpyruvate Sugar Phosphotransferase System EC 2.7.1.-
Glucose IY9XDZ35W2

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

122-136

Informations de copyright

© 2021 Society for Applied Microbiology and John Wiley & Sons Ltd.

Références

Brechemier-Baey, D., Pennetier, C., and Plumbridge, J. (2015) Dual inducer signal recognition by an Mlc homologue. Microbiology 161: 1694-1706.
Bross, M.H., Soch, K., Morales, R., and Mitchell, R.B. (2007) Vibrio vulnificus infection: diagnosis and treatment. Am Fam Physician 76: 539-544.
Choi, S.H., Lee, K.L., Shin, J.H., Cho, Y.B., Cha, S.S., and Roe, J.H. (2017) Zinc-dependent regulation of zinc import and export genes by Zur. Nat Commun 8: 15812.
Chowdhury, N.R., Chakraborty, S., Ramamurthy, T., Nishibuchi, M., Yamasaki, S., Takeda, Y., and Nair, G.B. (2000) Molecular evidence of clonal Vibrio parahaemolyticus pandemic strains. Emerg Infect Dis 6: 631-636.
Collado-Vides, J., Magasanik, B., and Gralla, J.D. (1991) Control site location and transcriptional regulation in Escherichia coli. Microbiol Rev 55: 371-394.
Decker, K., Plumbridge, J., and Boos, W. (1998) Negative transcriptional regulation of a positive regulator: the expression of malT, encoding the transcriptional activator of the maltose regulon of Escherichia coli, is negatively controlled by Mlc. Mol Microbiol 27: 381-390.
Deutscher, J., Ake, F.M., Derkaoui, M., Zebre, A.C., Cao, T.N., Bouraoui, H., et al. (2014) The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein-protein interactions. Microbiol Mol Biol Rev 78: 231-256.
Faruque, S.M., Albert, M.J., and Mekalanos, J.J. (1998) Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62: 1301-1314.
Ferenci, T. (1996) Adaptation to life at micromolar nutrient levels: the regulation of Escherichia coli glucose transport by endoinduction and cAMP. FEMS Microbiol Rev 18: 301-317.
Ghosh, S., Rao, K.H., Sengupta, M., Bhattacharya, S.K., and Datta, A. (2011) Two gene clusters co-ordinate for a functional N-acetylglucosamine catabolic pathway in Vibrio cholerae. Mol Microbiol 80: 1549-1560.
Gorke, B., and Stulke, J. (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6: 613-624.
Hayes, C.A., Dalia, T.N., and Dalia, A.B. (2017) Systematic genetic dissection of PTS in Vibrio cholerae uncovers a novel glucose transporter and a limited role for PTS during infection of a mammalian host. Mol Microbiol 104: 568-579.
Heo, K., Park, Y.H., Lee, K.A., Kim, J., Ham, H.I., Kim, B.G., et al. (2019) Sugar-mediated regulation of a c-di-GMP phosphodiesterase in Vibrio cholerae. Nat Commun 10: 5358.
Hirano, T., Okubo, M., Tsuda, H., Yokoyama, M., Hakamata, W., and Nishio, T. (2019) Chitin heterodisaccharide, released from chitin by chitinase and chitin oligosaccharide deacetylase, enhances the chitin-metabolizing ability of Vibrio parahaemolyticus. J Bacteriol 201: e00270-19.
Hogema, B.M., Arents, J.C., Bader, R., Eijkemans, K., Yoshida, H., Takahashi, H., et al. (1998) Inducer exclusion in Escherichia coli by non-PTS substrates: the role of the PEP to pyruvate ratio in determining the phosphorylation state of enzyme IIAGlc. Mol Microbiol 30: 487-498.
Houot, L., Chang, S., Pickering, B.S., Absalon, C., and Watnick, P.I. (2010) The phosphoenolpyruvate phosphotransferase system regulates Vibrio cholerae biofilm formation through multiple independent pathways. J Bacteriol 192: 3055-3067.
Hunt, D.E., Gevers, D., Vahora, N.M., and Polz, M.F. (2008) Conservation of the chitin utilization pathway in the Vibrionaceae. Appl Environ Microbiol 74: 44-51.
Jeong, J.Y., Kim, Y.J., Cho, N., Shin, D., Nam, T.W., Ryu, S., and Seok, Y.J. (2004) Expression of ptsG encoding the major glucose transporter is regulated by ArcA in Escherichia coli. J Biol Chem 279: 38513-38518.
Jones-Mortimer, M.C., and Kornberg, H.L. (1980) Amino-sugar transport systems of Escherichia coli K12. J Gen Microbiol 117: 369-376.
Karimova, G., Pidoux, J., Ullmann, A., and Ladant, D. (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756.
Kim, H.M., Park, Y.H., Yoon, C.K., and Seok, Y.J. (2015) Histidine phosphocarrier protein regulates pyruvate kinase A activity in response to glucose in Vibrio vulnificus. Mol Microbiol 96: 293-305.
Kim, H.M., Yoon, C.K., Ham, H.I., Seok, Y.J., and Park, Y.H. (2018) Stimulation of Vibrio vulnificus pyruvate kinase in the presence of glucose to cope with H2O2 stress generated by its competitors. Front Microbiol 9: 1112.
Kim, S.Y., Nam, T.W., Shin, D., Koo, B.M., Seok, Y.J., and Ryu, S. (1999) Purification of Mlc and analysis of its effects on the pts expression in Escherichia coli. J Biol Chem 274: 25398-25402.
Kim, Y.J., Ryu, Y., Koo, B.M., Lee, N.Y., Chun, S.J., Park, S.J., et al. (2010) A mammalian insulysin homolog is regulated by enzyme IIA(Glc) of the glucose transport system in Vibrio vulnificus. FEBS Lett 584: 4537-4544.
Kimata, K., Inada, T., Tagami, H., and Aiba, H. (1998) A global repressor (Mlc) is involved in glucose induction of the ptsG gene encoding major glucose transporter in Escherichia coli. Mol Microbiol 29: 1509-1519.
Kimata, K., Takahashi, H., Inada, T., Postma, P., and Aiba, H. (1997) cAMP receptor protein-cAMP plays a crucial role in glucose-lactose diauxie by activating the major glucose transporter gene in Escherichia coli. Proc Natl Acad Sci USA 94: 12914-12919.
Lee, C.R., Park, Y.H., Min, H., Kim, Y.R., and Seok, Y.J. (2019) Determination of protein phosphorylation by polyacrylamide gel electrophoresis. J Microbiol 57: 93-100.
Lee, K.J., Jeong, C.S., An, Y.J., Lee, H.J., Park, S.J., Seok, Y.J., et al. (2011) FrsA functions as a cofactor-independent decarboxylase to control metabolic flux. Nat Chem Biol 7: 434-436.
Lee, S.J., Boos, W., Bouche, J.P., and Plumbridge, J. (2000) Signal transduction between a membrane-bound transporter, PtsG, and a soluble transcription factor, Mlc, of Escherichia coli. EMBO J 19: 5353-5361.
Lim, J.G., Bang, Y.J., and Choi, S.H. (2014) Characterization of the Vibrio vulnificus 1-Cys peroxiredoxin Prx3 and regulation of its expression by the Fe-S cluster regulator IscR in response to oxidative stress and iron starvation. J Biol Chem 289: 36263-36274.
Meibom, K.L., Li, X.B., Nielsen, A.T., Wu, C.Y., Roseman, S., and Schoolnik, G.K. (2004) The Vibrio cholerae chitin utilization program. Proc Natl Acad Sci USA 101: 2524-2529.
Meins, M., Jeno, P., Muller, D., Richter, W.J., Rosenbusch, J.P., and Erni, B. (1993) Cysteine phosphorylation of the glucose transporter of Escherichia coli. J Biol Chem 268: 11604-11609.
Miller, J. (1972) Assay of B-galactosidase. In Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Nam, T.W., Cho, S.H., Shin, D., Kim, J.H., Jeong, J.Y., Lee, J.H., et al. (2001) The Escherichia coli glucose transporter enzyme IICB(Glc) recruits the global repressor Mlc. EMBO J 20: 491-498.
Nam, T.W., Jung, H.I., An, Y.J., Park, Y.H., Lee, S.H., Seok, Y.J., and Cha, S.S. (2008) Analyses of Mlc-IIBGlc interaction and a plausible molecular mechanism of Mlc inactivation by membrane sequestration. Proc Natl Acad Sci USA 105: 3751-3756.
Nam, T.W., Park, Y.H., Jeong, H.J., Ryu, S., and Seok, Y.J. (2005) Glucose repression of the Escherichia coli sdhCDAB operon, revisited: regulation by the CRP*cAMP complex. Nucleic Acids Res 33: 6712-6722.
Neiman, J., Guo, Y., and Rowe-Magnus, D.A. (2011) Chitin-induced carbotype conversion in Vibrio vulnificus. Infect Immun 79: 3195-3203.
Park, S., Park, Y.H., Lee, C.R., Kim, Y.R., and Seok, Y.J. (2016) Glucose induces delocalization of a flagellar biosynthesis protein from the flagellated pole. Mol Microbiol 101: 795-808.
Park, S., Yoon, J., Lee, C.R., Lee, J.Y., Kim, Y.R., Jang, K.S., et al. (2019) Polar landmark protein HubP recruits flagella assembly protein FapA under glucose limitation in Vibrio vulnificus. Mol Microbiol 112: 266-279.
Park, Y.H., Lee, C.R., Choe, M., and Seok, Y.J. (2013) HPr antagonizes the anti-sigma70 activity of Rsd in Escherichia coli. Proc Natl Acad Sci USA 110: 21142-21147.
Plumbridge, J. (1998a) Control of the expression of the manXYZ operon in Escherichia coli: Mlc is a negative regulator of the mannose PTS. Mol Microbiol 27: 369-380.
Plumbridge, J. (1998b) Expression of ptsG, the gene for the major glucose PTS transporter in Escherichia coli, is repressed by Mlc and induced by growth on glucose. Mol Microbiol 29: 1053-1063.
Plumbridge, J. (1999) Expression of the phosphotransferase system both mediates and is mediated by Mlc regulation in Escherichia coli. Mol Microbiol 33: 260-273.
Plumbridge, J. (2001) DNA binding sites for the Mlc and NagC proteins: regulation of nagE, encoding the N-acetylglucosamine-specific transporter in Escherichia coli. Nucleic Acids Res 29: 506-514.
Plumbridge, J.A. (1991) Repression and induction of the nag regulon of Escherichia coli K-12: the roles of nagC and nagA in maintenance of the uninduced state. Mol Microbiol 5: 2053-2062.
Postma, P.W., Lengeler, J.W., and Jacobson, G.R. (1993) Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57: 543-594.
Rungrassamee, W., Liu, X., and Pomposiello, P.J. (2008) Activation of glucose transport under oxidative stress in Escherichia coli. Arch Microbiol 190: 41-49.
Saier, M.H., Jr. (1977) Bacterial phosphoenolpyruvate: sugar phosphotransferase systems: structural, functional, and evolutionary interrelationships. Bacteriol Rev 41: 856-871.
Saier, M.H., Hvorup, R.N., and Barabote, R.D. (2005) Evolution of the bacterial phosphotransferase system: from carriers and enzymes to group translocators. Biochem Soc Trans 33: 220-224.
Seok, Y.J., Sondej, M., Badawi, P., Lewis, M.S., Briggs, M.C., Jaffe, H., and Peterkofsky, A. (1997) High affinity binding and allosteric regulation of Escherichia coli glycogen phosphorylase by the histidine phosphocarrier protein, HPr. J Biol Chem 272: 26511-26521.
Shin, D., Cho, N., Heu, S., and Ryu, S. (2003) Selective regulation of ptsG expression by Fis. Formation of either activating or repressing nucleoprotein complex in response to glucose. J Biol Chem 278: 14776-14781.
Stock, J.B., Waygood, E.B., Meadow, N.D., Postma, P.W., and Roseman, S. (1982) Sugar transport by the bacterial phosphotransferase system. The glucose receptors of the Salmonella typhimurium phosphotransferase system. J Biol Chem 257: 14543-14552.
Tanaka, Y., Kimata, K., and Aiba, H. (2000) A novel regulatory role of glucose transporter of Escherichia coli: membrane sequestration of a global repressor Mlc. EMBO J 19: 5344-5352.
Tanaka, Y., Kimata, K., Inada, T., Tagami, H., and Aiba, H. (1999) Negative regulation of the pts operon by Mlc: mechanism underlying glucose induction in Escherichia coli. Genes Cells 4: 391-399.
Thompson, F.L., Neto, A.A., Santos Ede, O., Izutsu, K., and Iida, T. (2011) Effect of N-acetyl-d-glucosamine on gene expression in Vibrio parahaemolyticus. Microbes Environ 26: 61-66.
Williams, K.P., Gillespie, J.J., Sobral, B.W., Nordberg, E.K., Snyder, E.E., Shallom, J.M., and Dickerman, A.W. (2010) Phylogeny of gammaproteobacteria. J Bacteriol 192: 2305-2314.
Yu, C., Bassler, B.L., and Roseman, S. (1993) Chemotaxis of the marine bacterium Vibrio furnissii to sugars. A potential mechanism for initiating the chitin catabolic cascade. J Biol Chem 268: 9405-9409.
Yu, C., Lee, A.M., Bassler, B.L., and Roseman, S. (1991) Chitin utilization by marine bacteria. A physiological function for bacterial adhesion to immobilized carbohydrates. J Biol Chem 266: 24260-24267.
Zheng, D., Constantinidou, C., Hobman, J.L., and Minchin, S.D. (2004) Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res 32: 5874-5893.

Auteurs

Ji-Hee Yoon (JH)

Department of Biophysics and Chemical Biology, Seoul National University, Seoul, South Korea.

Min-Seung Jeon (MS)

Department of Life Science, Chung-Ang University, Seoul, South Korea.

Seong-Il Eyun (SI)

Department of Life Science, Chung-Ang University, Seoul, South Korea.

Yeong-Jae Seok (YJ)

Department of Biophysics and Chemical Biology, Seoul National University, Seoul, South Korea.
School of Biological Sciences and Institute of Microbiology, Seoul National University, Seoul, South Korea.

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