MreB, the cell shape‐determining bacterial actin homologue, co‐ordinates cell wall morphogenesis in Caulobacter crescentus

The bacterial actin homologue, MreB, is required for the maintenance of a rod‐shaped cell and has been shown to form spirals that traverse along the longitudinal axis of Bacillus subtilis and Escherichia coli cells. The depletion of MreB in Caulobacter crescentus resulted in lemon‐shaped cells that possessed defects in the integrity of the cell wall. MreB localization appeared as bands or spirals that encircled the cell along its entire length and switched to a mid‐cell location at a time that coincided with the initiation of cell division. The formation of smaller MreB spirals or bands at the mid‐cell was dependent on the presence on the cytokinetic protein, FtsZ. Penicillin‐binding protein 2 (PBP2) also formed band‐like structures perpendicular to the cell periphery that resembled, and depended upon, MreB localization. PBP2 co‐immunoprecipitated with several other penicillin‐binding proteins, suggesting that these proteins are in association in Caulobacter cells. We hypothesize that MreB filaments function as a cytoskeleton that serves as an organizer or tracking device for the PBP2–peptidoglycan biosynthesis complex.

[1]  R. Doolittle,et al.  Bacterial actins? An evolutionary perspective. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[2]  M. Matsuhashi,et al.  Negative control of cell division by mreB, a gene that functions in determining the rod shape of Escherichia coli cells , 1989, Journal of bacteriology.

[3]  J. Höltje,et al.  Cloning and Characterization of PBP 1C, a Third Member of the Multimodular Class A Penicillin-binding Proteins of Escherichia coli * , 1999, The Journal of Biological Chemistry.

[4]  J. Kato,et al.  On the process of cellular division in Escherichia coli: Nucleotide sequence of the gene for penicillin-binding protein 3 , 2004, Molecular and General Genetics MGG.

[5]  Y. Brun,et al.  A set of ftsZ mutants blocked at different stages of cell division in Caulobacter , 2001, Molecular microbiology.

[6]  Y. Okada,et al.  Alteration in penicillin-binding patterns during cell cycle of Caulobacter crescentus. , 1984, Journal of Biochemistry (Tokyo).

[7]  G. Satta,et al.  Control of cell septation by lateral wall extension in a pH-conditional morphology mutant of Klebsiella pneumoniae , 1980, Journal of bacteriology.

[8]  M. Rees.  Relativistic jets and beams in radio galaxies , 1978, Nature.

[9]  N. Nanninga,et al.  Rate and topography of peptidoglycan synthesis during cell division in Escherichia coli: concept of a leading edge , 1989, Journal of bacteriology.

[10]  G. Stewart,et al.  The divIVB region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (minCD) and cell shape (mreBCD) determinants , 1992, Journal of bacteriology.

[11]  Y. Sakagami,et al.  Determinations of the DNA sequence of the mreB gene and of the gene products of the mre region that function in formation of the rod shape of Escherichia coli cells , 1988, Journal of bacteriology.

[12]  B. Spratt,et al.  Penicillin-binding proteins and cell shape in E. coli , 1975, Nature.

[13]  N. Agabian,et al.  Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells , 1977, Journal of bacteriology.

[14]  W. Donachie,et al.  Cell shape and division in Escherichia coli: experiments with shape and division mutants , 1985, Journal of bacteriology.

[15]  N. Nanninga.  Cell division and peptidoglycan assembly in Escherichia coli. , 1991, Molecular microbiology.

[16]  Yu-Ling Shih,et al.  Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  B. Spratt.  Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Gober,et al.  Cell Cycle–Dependent Polar Localization of Chromosome Partitioning Proteins in Caulobacter crescentus , 1997, Cell.

[19]  Y. Okada,et al.  The penicillin-binding proteins of Caulobacter crescentus. , 1980, Journal of biochemistry.

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

[21]  L. Shapiro,et al.  Differential expression and positioning of chemotaxis methylation proteins in Caulobacter. , 1984, Journal of molecular biology.

[22]  C. Hale,et al.  Direct Binding of FtsZ to ZipA, an Essential Component of the Septal Ring Structure That Mediates Cell Division in E. coli , 1997, Cell.

[23]  S. Tamaki,et al.  Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in Escherichia coli , 1987, Journal of bacteriology.

[24]  M. de Pedro,et al.  Murein segregation in Escherichia coli , 1997, Journal of bacteriology.

[25]  W. Margolin,et al.  Themes and variations in prokaryotic cell division. , 2000, FEMS microbiology reviews.

[26]  T D Pollard,et al.  Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. , 2000, Annual review of biophysics and biomolecular structure.

[27]  A. Bretscher,et al.  Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. , 2000, Journal of cell science.

[28]  A. Newton,et al.  Identification of two new cell division genes that affect a high-molecular-weight penicillin-binding protein in Caulobacter crescentus , 1988, Journal of bacteriology.

[29]  R. Losick,et al.  Identification of Bacillus subtilis genes for septum placement and shape determination , 1992, Journal of bacteriology.

[30]  W. Donachie,et al.  Identification of FtsW and characterization of a new ftsW division mutant of Escherichia coli , 1994, Journal of bacteriology.

[31]  L. Shapiro,et al.  Identification of the fliI and fliJ components of the Caulobacter flagellar type III protein secretion system , 1997, Journal of bacteriology.

[32]  J. Errington,et al.  Control of Cell Shape in Bacteria Helical, Actin-like Filaments in Bacillus subtilis , 2001, Cell.

[33]  L. Shapiro,et al.  Isolation and characterization of a xylose-dependent promoter from Caulobacter crescentus , 1997, Journal of bacteriology.

[34]  C. Koehler,et al.  Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. , 1998, Science.

[35]  H. Matsuzawa,et al.  Cluster of mrdA and mrdB genes responsible for the rod shape and mecillinam sensitivity of Escherichia coli , 1980, Journal of bacteriology.

[36]  A. Bretscher,et al.  Polarization of cell growth in yeast. , 2000, Journal of cell science.

[37]  J. Errington,et al.  Control of Cell Morphogenesis in Bacteria Two Distinct Ways to Make a Rod-Shaped Cell , 2003, Cell.

[38]  Y. Brun,et al.  Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. , 1998, Genes & development.

[39]  Jan Löwe,et al.  Prokaryotic origin of the actin cytoskeleton , 2001, Nature.

[40]  W. Vollmer,et al.  Demonstration of Molecular Interactions between the Murein Polymerase PBP1B, the Lytic Transglycosylase MltA, and the Scaffolding Protein MipA of Escherichia coli * , 1999, The Journal of Biological Chemistry.

[41]  N. Nanninga,et al.  Penicillin‐binding protein PBP2 of Escherichia coli localizes preferentially in the lateral wall and at mid‐cell in comparison with the old cell pole , 2003, Molecular microbiology.

[42]  M. Ikeda,et al.  New mutations fts-36, lts-33, and ftsW clustered in the mra region of the Escherichia coli chromosome induce thermosensitive cell growth and division , 1989, Journal of bacteriology.