On the Growth and Form of Free

Abstract

The shape of many micro-organisms can be understood in terms of the general surface stress hypothesis that hydrostatic pressure forces newly formed wall to expand in a particular direction. What distinguishes one type of organism from another is the regions of the cell where new wall growth occurs. For several classes of organisms, the pattern of growth deduced from the shape agrees with biochemical, morphological and physiological studies. Gram-negative rods, as typified by , have a morphology that may be explained in several ways by this general hypothesis.

In the present paper, the morphological, autoradiographic and biochemical data concerning are reviewed. Thirteen models are considered; there is reason to reject most of them but one model that includes two others appears more satisfactory. All the models conform to the biophysical principles that it is impossible to turn over stress-bearing peptidoglycan without shape change and that growth of the sacculus requires the introduction of new oligosaccharides and their covalent linkage before cleavage of stress-bearing bonds. The model that best accounts for the experimental data assumes that, while addition of peptidoglycan all over the cell is possible and does occur, the effective surface tension is higher (and therefore the rate of wall growth is very small) in old poles than on the sides, and very much lower at the developing division sites (where the rate of wall growth is high). It is shown that, when the hydrostatic pressure is constant throughout the cell and during a large part of the cell cycle, changes in the biochemical mechanism of wall growth which correspond to a decrease in surface tension would lead to an invagination of the stress-bearing wall. An additional mechanism may, however, be needed for final closure and for the splitting of the last few covalent bonds holding the two nascent cells together.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-128-11-2527
1982-11-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/128/11/mic-128-11-2527.html?itemId=/content/journal/micro/10.1099/00221287-128-11-2527&mimeType=html&fmt=ahah

References

  1. Boys C. V. 1890 Soap Bubbles and the Forces which Mould Them Society for the Promotion of Christian Knowledge London: Reprinted by Dover: New York; 1959
    [Google Scholar]
  2. Braun V. 1975; Covalent lipoprotein from the outer membrane of Escherichia coli. Biochimica et biophysica acta 415:335–377
    [Google Scholar]
  3. Burdett I. D. J., Higgins M. L. 1978; Studies of pole assembly in Bacillus subtilis by computer reconstructions of septal growth zones seen in central, longitudinal, thin sections of cells. Journal of Bacteriology 133:959–971
    [Google Scholar]
  4. Burdett I. D. J., Murray R. G. E. 1974a; Septum formation in Escherichia coli: characterization of septal structures and the effect of antibiotics on cell division. Journal of Bacteriology 119:303–324
    [Google Scholar]
  5. Burdett I. D. J., Murray R. G. E. 1974b; Electron microscope studies of septum formation in Escherichia coli strains B and B/r during synchronous growth. Journal of Bacteriology 119:1039–1056
    [Google Scholar]
  6. Cooper S., Helmstetter C. E. 1968; Chromosome replication and division cycle of Escherichia coli. Journal of Molecular Biology 31:519–540
    [Google Scholar]
  7. Daneo-Moore L., Shockman G. D. 1977; The bacterial cell surface in growth and division. In The Synthesis, Assembly and Turnover of Cell Surface Components pp. 597–715 Poste G., Nicolson G. L. Edited by Amsterdam: Elsevier/NorthHolland;
    [Google Scholar]
  8. De Pedro M. A., Schwarz U. 1981; Heterogeneity of newly inserted and pre-existing murein in the sacculus of E. coli. Proceedings of the National Academy of Sciences of the United States of America 78:5856–5860
    [Google Scholar]
  9. Grover N. B., Woldringh C. L., Zaritsky A., Rosenberger R. F. 1978; Elongation of rodshaped bacteria. Journal of Theoretical Biology 67:181–193
    [Google Scholar]
  10. Helmstetter C. E., Pierucci O., Weinberger M., Holmes M., Tang M. S. 1979; Control of cell division in Escherichia coli. In The Bacteria VII pp. 517–579 Gunsalus I. C., Stanier R. Y. Edited by New York: Academic Press;
    [Google Scholar]
  11. Higgins M. L., Shockman G. D. 1976; Study of a cycle of cell wall assembly in Streptococcus faecalis by three-dimensional reconstructions of thin section of cells. Journal of Bacteriology 127:1346–1358
    [Google Scholar]
  12. Hoffman B., Messer W., Schwarz U. 1972; Regulation of polar cap formation in the life cycle of Escherichia coli. Journal of Supramolecular Structure 1:29–37
    [Google Scholar]
  13. Koch A. L. 1977; Does the initiation of chromosome replication regulate cell division?. Advances in Microbial Physiology 16:49–98
    [Google Scholar]
  14. Koch A. L. 1982; The shape of the hyphal tips of fungi. Journal of General Microbiology 128:947–951
    [Google Scholar]
  15. Koch A. L., Higgins M. L. 1982; Cell cycle dynamics inferred from the static properties of cells in balanced growth. Journal of General Microbiology in the Press
    [Google Scholar]
  16. Koch A. L., Higgins M. L., Doyle R. J. 1981a; Surface tension-like forces determine bacterial shapes: Streptococcus faecium. Journal of General Microbiology 123:151–161
    [Google Scholar]
  17. Koch A. L., Mobley H. L. T., Doyle R. J., Streips U. N. 1981b; The coupling of wall growth and chromosome replication in Gram positive rods. FEMS Microbiology Letters 12:201–208
    [Google Scholar]
  18. Koch A. L., Higgins M. L., Doyle R. J. 1982; The role of surface stress in the morphology of microbes. Journal of General Microbiology 128:927–945
    [Google Scholar]
  19. Koppes L. J. H., Woldringh C. L., Nanninga N. 1978; Size variation and correlation of different cell cycle events in slow-growing Escherichia coli. Journal of Bacteriology 134:423–433
    [Google Scholar]
  20. Lark K. G. 1978; Some aspects of the regulation of DNA replication in Escherichia coli. In Biological Control and Development pp. 201–217 Goldberger R. F. Edited by New York: Plenum Press;
    [Google Scholar]
  21. Lin E. C. C., Hirota Y., Jacob F. 1971; On the process of cellular division in Escherichia coli. VI. Use of a Methocel-autoradiographic method for the study of cellular division in Escherichia coli. Journal of Bacteriology 108:375–385
    [Google Scholar]
  22. MaalØe O. 1978; Regulation of protein synthesizing machinery-ribosomes, rRNA, factors, etc. In Biological Control and Development pp. 487–542 Goldberger R. F. Edited by New York: Plenum Press;
    [Google Scholar]
  23. Maaløe O., Kjeldgaard N. O. 1966 Control of Macromolecular Synthesis New York: W. A. Benjamin;
    [Google Scholar]
  24. Plateau J. A. F. 1873 Statique Expérimental et Théorique des LiquidesSoumis aux Seules Forces Moléculaire Paris: Gauthier-Villars;
    [Google Scholar]
  25. Pritchard R. H. 1974; On the growth and form of a bacterial cell. Philosophical Transactions of the Royal Society B267:303–336
    [Google Scholar]
  26. Ryter A., Hirota Y., Schwarz U. 1973; Process of cellular division in Escherichia coli. Growth pattern of E. colimurein. Journal of Molecular Biology 78:185–195
    [Google Scholar]
  27. Sargent M. 1979; Surface extension and the cell cycle in prokaryotes. Advances in Microbial Physiology 18:105–176
    [Google Scholar]
  28. Schaechter M., Williamson J. P., Hood J. R. Jr Koch A. L. 1962; Growth, cell and nuclear divisions in some bacteria. Journal of General Microbiology 29:421–434
    [Google Scholar]
  29. Schwarz U., Asmus A., Frank H. 1969; Autolytic enzymes and cell division of Escherichia coli. Journal of Molecular Biology 41:419–429
    [Google Scholar]
  30. Schwarz U., Ryter A., Rambach A., Hellio R., Hirota Y. 1975; Process of cellular division in Escherichia coli. Differentiation of growth zones in the sacculus. Journal of Molecular Biology 98:749–759
    [Google Scholar]
  31. Thompson, D’Arcy W. 1942 On Growth and Form, 2nd edn. pp. 351–384 Cambridge: Cambridge University Press;
    [Google Scholar]
  32. Trueba F. J., Woldringh C. L. 1980; Changes in cell diameter during the division cycle of Escherichia coli. Journal of Bacteriology 142:869–878
    [Google Scholar]
  33. Van Tubergen R. P., Setlow R. B. 1961; Quantitative radioautographic studies of exponentially growing cultures of Escherichia coli. Biophysical Journal 1:589–625
    [Google Scholar]
  34. Verwer R. W. H., Nanninga N. 1980; Pattern of meso-dl-2,6-diaminopimelic acid incorporation during the division cycle of Escherichia coli. Journal of Bacteriology 144:327–336
    [Google Scholar]
  35. Woldringh C. L., De Jong M. A., Van Den Berg W., Koppes L. 1977; Morphological analysis of the division cycle of two Escherichia colisubstrains during slow growth. Journal of Bacteriology 131:270–279
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-128-11-2527
Loading
/content/journal/micro/10.1099/00221287-128-11-2527
Loading

Data & Media loading...

Most cited Most Cited RSS feed