Novel regulator PgrR for switch control of peptidoglycan recycling in Escherichia coli

Peptidoglycan (PG), also designated as murein, forms a skeletal mesh within the periplasm of bacterial membrane. PG is a metabolically stable cell architecture in Escherichia coli, but under as yet ill‐defined conditions, a portion of PG is degraded, of which both amino sugar and peptide moieties are either recycled or used as self‐generated nutrients for cell growth. At present, the control of PG degradation remains uncharacterized. Using the Genomic SELEX screening system, we identified an uncharacterized transcription factor YcjZ is a repressor of the expression of the initial step enzymes for PG peptide degradation. Under nutrient starvation, the genes encoding the enzymes for PG peptide degradation are derepressed so as to generate amino acids but are tightly repressed at high osmotic conditions so as to maintain the rigid membrane for withstanding the turgor. Taken together, we propose to rename YcjZ as PgrR (regulator of peptide glycan recycling).

[1]  U. Schwarz,et al.  Release of cell wall peptides into culture medium by exponentially growing Escherichia coli , 1985, Journal of bacteriology.

[2]  Akira Ishihama,et al.  Systematic search for the Cra‐binding promoters using genomic SELEX system , 2005, Genes to cells : devoted to molecular & cellular mechanisms.

[3]  M. de Pedro,et al.  Normal growth and division of Escherichia coli with a reduced amount of murein , 1989, Journal of bacteriology.

[4]  A. Ishihama,et al.  The Uncharacterized Transcription Factor YdhM Is the Regulator of the nemA Gene, Encoding N-Ethylmaleimide Reductase , 2008, Journal of bacteriology.

[5]  James T. Park,et al.  How Bacteria Consume Their Own Exoskeletons (Turnover and Recycling of Cell Wall Peptidoglycan) , 2008, Microbiology and Molecular Biology Reviews.

[6]  V. Braun,et al.  Transcriptional regulation of ferric citrate transport in Escherichia coli K‐12. Fecl belongs to a new subfamily of σ70‐type factors that respond to extracytoplasmic stimuli , 1995, Molecular microbiology.

[7]  L. Glaser,et al.  Turnover of the cell wall of Gram-positive bacteria. , 1971, The Journal of biological chemistry.

[8]  Takashi Yura,et al.  Convergence of Molecular, Modeling, and Systems Approaches for an Understanding of the Escherichia coli Heat Shock Response , 2008, Microbiology and Molecular Biology Reviews.

[9]  Jeffrey H. Miller Experiments in molecular genetics , 1972 .

[10]  Akira Ishihama,et al.  A novel regulator RcdA of the csgD gene encoding the master regulator of biofilm formation in Escherichia coli , 2012, MicrobiologyOpen.

[11]  Akira Ishihama,et al.  Genomic SELEX Search for Target Promoters under the Control of the PhoQP-RstBA Signal Relay Cascade , 2007, Journal of bacteriology.

[12]  J. Höltje,et al.  Growth of the Stress-Bearing and Shape-Maintaining Murein Sacculus of Escherichia coli , 1998, Microbiology and Molecular Biology Reviews.

[13]  James T. Park,et al.  Identification of MpaA, an Amidase in Escherichia coli That Hydrolyzes the γ-d-Glutamyl-meso-Diaminopimelate Bond in Murein Peptides , 2003, Journal of bacteriology.

[14]  A. Ishihama Prokaryotic genome regulation: A revolutionary paradigm , 2012, Proceedings of the Japan Academy. Series B, Physical and biological sciences.

[15]  A. Ishihama Functional modulation of Escherichia coli RNA polymerase. , 2000, Annual review of microbiology.

[16]  C. Gross,et al.  Multiple sigma subunits and the partitioning of bacterial transcription space. , 2003, Annual review of microbiology.

[17]  B. Henrich,et al.  Peptidase D of Escherichia coli K-12, a metallopeptidase of low substrate specificity. , 1994, FEMS microbiology letters.

[18]  S. Normark,et al.  MppA, a Periplasmic Binding Protein Essential for Import of the Bacterial Cell Wall Peptidel-Alanyl-γ-d-Glutamyl-meso-Diaminopimelate , 1998, Journal of bacteriology.

[19]  Akira Ishihama,et al.  Modulation of the nucleoid, the transcription apparatus, and the translation machinery in bacteria for stationary phase survival , 1999, Genes to cells : devoted to molecular & cellular mechanisms.

[20]  Jan Barciszewski,et al.  Regulation by RNA. , 2003, International review of cytology.

[21]  R. Utsumi,et al.  Functional Characterization in Vitro of All Two-component Signal Transduction Systems from Escherichia coli* , 2005, Journal of Biological Chemistry.

[22]  E. Goodell Recycling of murein by Escherichia coli , 1985, Journal of bacteriology.

[23]  G. Thomas,et al.  MpaA is a murein-tripeptide-specific zinc carboxypeptidase that functions as part of a catabolic pathway for peptidoglycan-derived peptides in γ-proteobacteria. , 2012, The Biochemical journal.

[24]  B. Wanner,et al.  One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  T. D. Schneider,et al.  Small membrane proteins found by comparative genomics and ribosome binding site models , 2008, Molecular microbiology.

[26]  A. Ishihama,et al.  Novel roles of LeuO in transcription regulation of E. coli genome: antagonistic interplay with the universal silencer H‐NS , 2011, Molecular microbiology.

[27]  Akira Ishihama,et al.  A novel nucleoid protein of Escherichia coli induced under anaerobiotic growth conditions , 2010, Nucleic acids research.

[28]  Noelia Valbuena,et al.  Recycling of the Anhydro-N-Acetylmuramic Acid Derived from Cell Wall Murein Involves a Two-Step Conversion to N-Acetylglucosamine-Phosphate , 2005, Journal of bacteriology.

[29]  A. Ishihama,et al.  Novel Members of the Cra Regulon Involved in Carbon Metabolism in Escherichia coli , 2010, Journal of Bacteriology.

[30]  A. Ishihama Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks. , 2010, FEMS microbiology reviews.

[31]  N. Fujita,et al.  Novel Roles of cAMP Receptor Protein (CRP) in Regulation of Transport and Metabolism of Carbon Sources , 2011, PloS one.

[32]  H. Mori,et al.  Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection , 2006, Molecular systems biology.

[33]  Akira Ishihama,et al.  The Escherichia coli RutR transcription factor binds at targets within genes as well as intergenic regions , 2008, Nucleic acids research.

[34]  A. Ishihama,et al.  Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of sigma 70 and sigma 38 , 1995, Journal of bacteriology.

[35]  A. Ishihama,et al.  RutR is the uracil/thymine‐sensing master regulator of a set of genes for synthesis and degradation of pyrimidines , 2007, Molecular microbiology.

[36]  M. de Pedro,et al.  Peptidoglycan structure and architecture. , 2008, FEMS microbiology reviews.

[37]  The Bacteria , 1881, Nature.