Compartmentalization of the periplasm at cell division sites in Escherichia coli as shown by fluorescence photobleaching experiments

Morphological evidence has previously indicated that the periplasmic space of Escherichia coli is compartmentalized at sites corresponding to future sites of cell division. The borders of these morphological compartments are formed by localized zones of adhesion (periseptal annuli). In the present study, the technique of fluorescence recovery after photo‐bleaching was used to determine whether these structures act as barriers to the free movement of proteins within the periplasm. The recovery of fluorescence in the ftsA filaments was found to be uniformly low over at potential sites of cell division and at the cell poles, indicating that these regions are biochemically sequestered from the remainder of the periplasmic space. Our results provide direct evidence for local compartments within the periplasm, primarily located at the sites of past or future cell divisions. The implications of this finding for cell division and other periplasmic processes are discussed.

[1]  W. Cook,et al.  Compartmentalization of the periplasmic space at division sites in gram-negative bacteria , 1986, Journal of bacteriology.

[2]  R. Schauer,et al.  Analysis of sialidase and N-acetylneuraminate pyruvate-lyase substrate specificity by high-performance liquid chromatography. , 1986, Analytical biochemistry.

[3]  M. Foley,et al.  Lateral diffusion of proteins in the periplasm of Escherichia coli , 1986, Journal of bacteriology.

[4]  E. Kellenberger,et al.  Periplasmic gel: new concept resulting from the reinvestigation of bacterial cell envelope ultrastructure by new methods , 1984, Journal of bacteriology.

[5]  M. Manson,et al.  Reconstitution of maltose chemotaxis in Escherichia coli by addition of maltose-binding protein to calcium-treated cells of maltose regulon mutants , 1984, Journal of bacteriology.

[6]  B. Bukau,et al.  Reconstitution of maltose transport in Escherichia coli: conditions affecting import of maltose-binding protein into the periplasm of calcium-treated cells , 1983, Journal of bacteriology.

[7]  B. Lugtenberg,et al.  Molecular architecture and functioning of the outer membrane of Escherichia coli and other gram-negative bacteria. , 1983, Biochimica et biophysica acta.

[8]  L. Rothfield,et al.  The periseptal annulus: An organelle associated with cell division in Gram-negative bacteria. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[9]  M. T. Davison,et al.  Immunochemical demonstration of zonal growth of the cell envelope of Escherichia coli. , 1983, European journal of biochemistry.

[10]  H. Shuman.  Active transport of maltose in Escherichia coli K12. Role of the periplasmic maltose-binding protein and evidence for a substrate recognition site in the cytoplasmic membrane. , 1982, The Journal of biological chemistry.

[11]  R. Peters.  Translational diffusion in the plasma membrane of single cells as studied by fluorescence microphotolysis. , 1981, Cell biology international reports.

[12]  P. Garland.  Fluorescence photobleaching recovery: control of laser intensities with an acousto-optic modulator. , 1981, Biophysical journal.

[13]  J. Lutkenhaus,et al.  Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ) , 1980, Journal of bacteriology.

[14]  D. Koppel,et al.  Lateral mobility in reconstituted membranes—comparisons with diffusion in polymers , 1980, Nature.

[15]  T. Ferenci,et al.  Affinity chromatographic isolation of the periplasmic maltose binding protein of Escherichia coli , 1978, FEBS letters.

[16]  W. Webb,et al.  Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. , 1976, Biophysical journal.

[17]  Y. Anraku,et al.  Transport of sugars and amino acids in bacteria. XVI. Theory and evaluation of a model for the membrane transport reaction mediated by a single carrier with three binding sites for substrate. , 1975, Journal of biochemistry.

[18]  Y. Anraku.  Transport of sugars and amino acids in bacteria. I. Purification and specificity of the galactose- and leucine-binding proteins. , 1968, The Journal of biological chemistry.

[19]  P. van de Putte,et al.  THE SELECTION OF MUTANTS OF ESCHERICHIA COLI WITH IMPAIRED CELL DIVISION AT ELEVATED TEMPERATURE. , 1964, Mutation research.

[20]  A. Ryter,et al.  Cell Wall and Cytoplasmic Membrane of Escherichia coli , 1958, The Journal of biophysical and biochemical cytology.

[21]  J. Brass.  The cell envelope of gram-negative bacteria: new aspects of its function in transport and chemotaxis. , 1986, Current topics in microbiology and immunology.

[22]  J. Brass.  Calcium-induced permeabilization of the outer membrane: a method for reconstitution of periplasmic binding protein-dependent transport systems in Escherichia coli and Salmonella typhimurium. , 1986, Methods in enzymology.

[23]  J. Pagés,et al.  The periseptal annulus in Escherichia coli , 1984, Biology of the cell.

[24]  V. Braun,et al.  Biochemistry of bacterial cell envelopes. , 1974, Annual review of biochemistry.