Diversity of Firmicutes peptidoglycan hydrolases and specificities of those involved in daughter cell separation.

Within Streptococcus thermophilus, Cse was identified as the major cell disconnecting peptidoglycan hydrolase (PGH) and was demonstrated to be species-specific. To identify cell disconnecting PGHs encoded by other Streptococcus genomes, we explored the diversity of domains carried by Firmicutes PGHs, and especially that of enzymes involved in daughter cell separation. This work brings to light the diversity of PGHs and reveals that each species recruits its own cell-separating enzyme distinct from that of the others. This specificity is probably correlated with the diversity of substrates found in the bacterial cell wall.

[1]  M. Sugai,et al.  An autolysin ring associated with cell separation of Staphylococcus aureus , 1996, Journal of bacteriology.

[2]  C. Thiemermann,et al.  The cell wall components peptidoglycan and lipoteichoic acid from Staphylococcus aureus act in synergy to cause shock and multiple organ failure. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[3]  O. Massidda,et al.  Bacterial walls, peptidoglycan hydrolases, autolysins, and autolysis. , 1996, Microbial drug resistance.

[4]  J. Sekiguchi,et al.  A New d,l-Endopeptidase Gene Product, YojL (Renamed CwlS), Plays a Role in Cell Separation with LytE and LytF in Bacillus subtilis , 2006, Journal of bacteriology.

[5]  S. Ishikawa,et al.  Peptidoglycan Hydrolase LytF Plays a Role in Cell Separation with CwlF during Vegetative Growth of Bacillus subtilis , 1999, Journal of bacteriology.

[6]  T. Chakraborty,et al.  Identification and Characterization of a Peptidoglycan Hydrolase, MurA, of Listeria monocytogenes, a Muramidase Needed for Cell Separation , 2003, Journal of bacteriology.

[7]  Ernesto García,et al.  Skl, a novel choline‐binding N‐acetylmuramoyl‐l‐alanine amidase of Streptococcus mitis SK137 containing a CHAP domain , 2006, FEBS letters.

[8]  Yoshika Suzawa,et al.  Identification and molecular characterization of an N‐acetylmuramyl‐l‐alanine amidase Sle1 involved in cell separation of Staphylococcus aureus , 2005, Molecular microbiology.

[9]  S. Moineau,et al.  Peptidoglycan Hydrolase Fusions Maintain Their Parental Specificities , 2006, Applied and Environmental Microbiology.

[10]  E. Díaz,et al.  Carboxy-terminal deletion analysis of the major pneumococcal autolysin , 1994, Journal of bacteriology.

[11]  John F. Kennedy,et al.  Bacterial cell wall , 1996 .

[12]  Identification and Molecular Characterization of an N‐Acetylmuraminidase, Aml, Involved in Streptococcus mutans Cell Separation , 2006, Microbiology and immunology.

[13]  M. Sugai,et al.  Cell Wall-targeting Domain of Glycylglycine Endopeptidase Distinguishes among Peptidoglycan Cross-bridges* , 2006, Journal of Biological Chemistry.

[14]  T. Butters,et al.  Cloning and expression of the beta-N-acetylglucosaminidase gene from Streptococcus pneumoniae. Generation of truncated enzymes with modified aglycon specificity. , 1995, The Journal of biological chemistry.

[15]  S. Foster,et al.  Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. , 2000, Microbiology.

[16]  Shogo Nakamura,et al.  The two-component cell lysis genes holWMY and lysWMY of the Staphylococcus warneri M phage varphiWMY: cloning, sequencing, expression, and mutational analysis in Escherichia coli. , 2005, Gene.

[17]  Bernard Decaris,et al.  Characterization of Proteins Belonging to the CHAP-Related Superfamily within the Firmicutes , 2007, Journal of Molecular Microbiology and Biotechnology.

[18]  S. Gillespie Gram-positive cocci , 1994 .

[19]  G. Raux,et al.  Acd, a peptidoglycan hydrolase of Clostridium difficile with N-acetylglucosaminidase activity. , 2005, Microbiology.

[20]  C. Croux,et al.  Interchange of functional domains switches enzyme specificity: construction of a chimeric pneumococcal‐clostridial cell wall lytic enzyme , 1993, Molecular microbiology.

[21]  S. Foster,et al.  Complete spore-cortex hydrolysis during germination of Bacillus subtilis 168 requires SleB and YpeB. , 2000, Microbiology.

[22]  R. Moriyama,et al.  A germination-specific spore cortex-lytic enzyme from Bacillus cereus spores: cloning and sequencing of the gene and molecular characterization of the enzyme , 1996, Journal of bacteriology.

[23]  Robert D. Finn,et al.  Pfam: clans, web tools and services , 2005, Nucleic Acids Res..

[24]  J. Engler,et al.  The bifunctional peptidoglycan lysin of Streptococcus agalactiae bacteriophage B30. , 2004, Microbiology.

[25]  M. Sugai,et al.  Mutation Analysis of the Histidine Residues in the Glycylglycine Endopeptidase ALE-1 , 2005, Journal of bacteriology.

[26]  J. Sekiguchi,et al.  Characterization of a new Bacillus subtilis peptidoglycan hydrolase gene, yvcE (named cwlO), and the enzymatic properties of its encoded protein. , 2004, Journal of bioscience and bioengineering.

[27]  S. Foster,et al.  Characterization of the involvement of two compensatory autolysins in mother cell lysis during sporulation of Bacillus subtilis 168 , 1995, Journal of bacteriology.

[28]  E. Díaz,et al.  Role of the major pneumococcal autolysin in the atypical response of a clinical isolate of Streptococcus pneumoniae , 1992, Journal of bacteriology.

[29]  J. Sánchez-Puelles,et al.  Cloning and expression of gene fragments encoding the choline-binding domain of pneumococcal murein hydrolases. , 1990, Gene.

[30]  M. Pagni,et al.  Bacillus subtilis 168 gene lytF encodes a γ-D-glutamate-meso-diaminopimelate muropeptidase expressed by the alternative vegetative sigma factor, σD , 1999 .

[31]  J. Sekiguchi,et al.  Localization of the Vegetative Cell Wall Hydrolases LytC, LytE, and LytF on the Bacillus subtilis Cell Surface and Stability of These Enzymes to Cell Wall-Bound or Extracellular Proteases , 2003, Journal of bacteriology.

[32]  Beatriz Galán,et al.  Structural basis for selective recognition of pneumococcal cell wall by modular endolysin from phage Cp-1. , 2003, Structure.

[33]  T. Vernet,et al.  Crystal Structure of a Peptidoglycan Synthesis Regulatory Factor (PBP3) from Streptococcus pneumoniae* , 2005, Journal of Biological Chemistry.

[34]  O. Schneewind,et al.  The YSIRK-G/S Motif of Staphylococcal Protein A and Its Role in Efficiency of Signal Peptide Processing , 2003, Journal of bacteriology.

[35]  G. Shockman Microbial peptidoglycan (murein) hydrolases , 1994 .

[36]  Aldert L. Zomer,et al.  Cell Wall Attachment of a Widely Distributed Peptidoglycan Binding Domain Is Hindered by Cell Wall Constituents* , 2003, Journal of Biological Chemistry.

[37]  R. Moriyama,et al.  A gene (sleB) encoding a spore cortex-lytic enzyme from Bacillus subtilis and response of the enzyme to L-alanine-mediated germination , 1996, Journal of bacteriology.

[38]  W. Goebel,et al.  The iap gene of Listeria monocytogenes is essential for cell viability, and its gene product, p60, has bacteriolytic activity , 1993, Journal of bacteriology.

[39]  F. Borges,et al.  cse, a Chimeric and Variable Gene, Encodes an Extracellular Protein Involved in Cellular Segregation in Streptococcus thermophilus , 2005, Journal of bacteriology.

[40]  P. Andrew,et al.  The role of pneumolysin and autolysin in the pathology of pneumonia and septicemia in mice infected with a type 2 pneumococcus. , 1995, The Journal of infectious diseases.

[41]  S. Foster,et al.  Molecular characterization of an autolytic amidase of Listeria monocytogenes EGD. , 1998, Microbiology.

[42]  J. García,et al.  Purification and Polar Localization of Pneumococcal LytB, a Putative Endo-β-N-Acetylglucosaminidase: the Chain-Dispersing Murein Hydrolase , 2002, Journal of bacteriology.

[43]  S. Ishikawa,et al.  Regulation of a New Cell Wall Hydrolase Gene,cwlF, Which Affects Cell Separation in Bacillus subtilis , 1998, Journal of bacteriology.

[44]  S. Foster,et al.  AcmA of Lactococcus lactis is an N‐acetylglucosaminidase with an optimal number of LysM domains for proper functioning , 2005, The FEBS journal.

[45]  E. Díaz,et al.  Chimeric phage-bacterial enzymes: a clue to the modular evolution of genes. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[46]  S. Brunak,et al.  Improved prediction of signal peptides: SignalP 3.0. , 2004, Journal of molecular biology.

[47]  M. Sugai,et al.  Purification and molecular characterization of glycylglycine endopeptidase produced by Staphylococcus capitis EPK1 , 1997, Journal of bacteriology.

[48]  G. Venema,et al.  Molecular cloning and nucleotide sequence of the gene encoding the major peptidoglycan hydrolase of Lactococcus lactis, a muramidase needed for cell separation , 1995, Journal of bacteriology.

[49]  M. Lecerf,et al.  Functional Analysis of AtlA, the Major N-Acetylglucosaminidase of Enterococcus faecalis , 2006, Journal of bacteriology.

[50]  K. Schleifer,et al.  Peptidoglycan types of bacterial cell walls and their taxonomic implications , 1972, Bacteriological reviews.

[51]  O. Schneewind,et al.  Multiple enzymatic activities of the murein hydrolase from staphylococcal phage phi11. Identification of a D-alanyl-glycine endopeptidase activity. , 1999, The Journal of biological chemistry.

[52]  F. Götz,et al.  Activity of the major staphylococcal autolysin Atl. , 2006, FEMS microbiology letters.

[53]  Gabriele Bierbaum,et al.  Lytic Activity of Recombinant Bacteriophage φ11 and φ12 Endolysins on Whole Cells and Biofilms of Staphylococcus aureus , 2006, Applied and Environmental Microbiology.

[54]  A M Lesk,et al.  SH3 domains in prokaryotes. , 1999, Trends in biochemical sciences.

[55]  P. Setlow,et al.  Roles of Low-Molecular-Weight Penicillin-Binding Proteins in Bacillus subtilis Spore Peptidoglycan Synthesis and Spore Properties , 1999, Journal of bacteriology.

[56]  J. García,et al.  Elucidation of the Molecular Recognition of Bacterial Cell Wall by Modular Pneumococcal Phage Endolysin CPL-1* , 2007, Journal of Biological Chemistry.

[57]  A. L. Koch The Bacterium's Way for Safe Enlargement and Division , 2000, Applied and Environmental Microbiology.

[58]  T. Vernet,et al.  The d,d‐carboxypeptidase PBP3 organizes the division process of Streptococcus pneumoniae , 2004, Molecular microbiology.

[59]  J. Sekiguchi,et al.  Nucleotide sequence and regulation of a new putative cell wall hydrolase gene, cwlD, which affects germination in Bacillus subtilis. , 1995, Journal of bacteriology.

[60]  Š. Janeček,et al.  Location of repeat elements in glucansucrases of Leuconostoc and Streptococcus species. , 2000, FEMS microbiology letters.

[61]  M. Bochtler,et al.  Folds and activities of peptidoglycan amidases. , 2007, FEMS microbiology reviews.

[62]  P. Cossart,et al.  The autolysin Ami contributes to the adhesion of Listeria monocytogenes to eukaryotic cells via its cell wall anchor , 2001, Molecular microbiology.

[63]  P. Cossart,et al.  InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association , 1997, Molecular microbiology.

[64]  P. Setlow,et al.  Muramic lactam in peptidoglycan of Bacillus subtilis spores is required for spore outgrowth but not for spore dehydration or heat resistance. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[65]  W. Goebel,et al.  Identification of an extracellular protein of Listeria monocytogenes possibly involved in intracellular uptake by mammalian cells , 1989, Infection and immunity.

[66]  E. Díaz,et al.  Chimeric pneumococcal cell wall lytic enzymes reveal important physiological and evolutionary traits. , 1991, The Journal of biological chemistry.

[67]  M. Rohde,et al.  Simultaneous Deficiency of both MurA and p60 Proteins Generates a Rough Phenotype in Listeria monocytogenes , 2005, Journal of bacteriology.

[68]  J. Ghuysen,et al.  Cloning and nucleotide sequence of the gene encoding the gamma-D-glutamyl-L-diamino acid endopeptidase II of Bacillus sphaericus. , 1992, FEMS microbiology letters.

[69]  J F Barrett,et al.  Structure, function, and assembly of cell walls of gram-positive bacteria. , 1983, Annual review of microbiology.

[70]  B. Eikmanns,et al.  Influence of proteins Bsp and FemH on cell shape and peptidoglycan composition in group B streptococcus. , 2002, Microbiology.

[71]  C. Kojima,et al.  Solution structure of the peptidoglycan binding domain of Bacillus subtilis cell wall lytic enzyme CwlC: characterization of the sporulation-related repeats by NMR. , 2005, Biochemistry.

[72]  M. G. Pinho,et al.  Bacterial Cell Wall Synthesis: New Insights from Localization Studies , 2005, Microbiology and Molecular Biology Reviews.

[73]  M. González,et al.  LytB, a novel pneumococcal murein hydrolase essential for cell separation , 1999, Molecular microbiology.

[74]  Neil D. Rawlings,et al.  Handbook of proteolytic enzymes , 1998 .

[75]  W. Goebel,et al.  Expression of the iap gene coding for protein p60 of Listeria monocytogenes is controlled on the posttranscriptional level , 1991, Journal of bacteriology.

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

[77]  D. Karamata,et al.  The lytE Gene of Bacillus subtilis 168 Encodes a Cell Wall Hydrolase , 1998, Journal of bacteriology.

[78]  Alex Bateman,et al.  The G5 domain: a potential N-acetylglucosamine recognition domain involved in biofilm formation , 2005, Bioinform..

[79]  A. Tomasz,et al.  A Staphylococcus aureus autolysin that has an N-acetylmuramoyl-L-alanine amidase domain and an endo-beta-N-acetylglucosaminidase domain: cloning, sequence analysis, and characterization. , 1995, Proceedings of the National Academy of Sciences of the United States of America.