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. 1988 Jan;170(1):422–430. doi: 10.1128/jb.170.1.422-430.1988

Rate and topography of cell wall synthesis during the division cycle of Salmonella typhimurium.

S Cooper 1
PMCID: PMC210659  PMID: 3275624

Abstract

The rates of synthesis of peptidoglycan and protein during the division cycle of Salmonella typhimurium have been measured by using the membrane elution technique and differentially labeled diaminopimelic acid and leucine. The cells were labeled during unperturbed exponential growth and then bound to a nitrocellulose membrane by filtration. Newborn cells were eluted from the membrane with fresh medium. The radioactivity in the newborn cells in successive fractions was determined. As the cells are eluted from the membrane as a function of their cell cycle age at the time of labeling, the rate of incorporation of the different radioactive compounds as a function of cell cycle age can be determined. During the first part of the division cycle, the ratio of the rates of protein and peptidoglycan synthesis was constant. During the latter part of the division cycle, there was an increase in the rate of peptidoglycan synthesis relative to the rate of protein synthesis. These results support a simple, bipartite model of cell surface increase in rod-shaped cells. Before the start of constriction, the cell surface increased only by cylindrical extension. After cell constriction started, the cell surface increased by both cylinder and pole growth. The increase in surface area was partitioned between the cylinder and the pole so that the volume of the cell increased exponentially. No variation in cell density occurred because the increase in surface allowed a continuous exponential increase in cell volume that accommodated the exponential increase in cell mass. Protein was synthesized exponentially during the division cycle. The rate of cell surface increase was described by a complex equation which is neither linear nor exponential.

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Selected References

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  1. Begg K. J., Doanachie W. D. Growth of the Escherichia coli cell surface. J Bacteriol. 1977 Mar;129(3):1524–1536. doi: 10.1128/jb.129.3.1524-1536.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burdett I. D., Kirkwood T. B. How does a bacterium grow during its cell cycle? J Theor Biol. 1983 Jul 7;103(1):11–20. doi: 10.1016/0022-5193(83)90195-9. [DOI] [PubMed] [Google Scholar]
  3. Burdett I. D., Murray R. G. Electron microscope study of septum formation in Escherichia coli strains B and B-r during synchronous growth. J Bacteriol. 1974 Sep;119(3):1039–1056. doi: 10.1128/jb.119.3.1039-1056.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burman L. G., Raichler J., Park J. T. Evidence for diffuse growth of the cylindrical portion of the Escherichia coli murein sacculus. J Bacteriol. 1983 Sep;155(3):983–988. doi: 10.1128/jb.155.3.983-988.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. COLLINS J. F., RICHMOND M. H. Rate of growth of Bacillus cereus between divisions. J Gen Microbiol. 1962 Apr;28:15–33. doi: 10.1099/00221287-28-1-15. [DOI] [PubMed] [Google Scholar]
  6. Chaloupka J., Strnadová M. Turnover of murein in a diaminopimelic acid dependent mutant of Escherichia coli. Folia Microbiol (Praha) 1972;17(6):446–455. doi: 10.1007/BF02872729. [DOI] [PubMed] [Google Scholar]
  7. Cooper S. Cell division and DNA replication following a shift to a richer medium. J Mol Biol. 1969 Jul 14;43(1):1–11. doi: 10.1016/0022-2836(69)90074-6. [DOI] [PubMed] [Google Scholar]
  8. Cooper S., Helmstetter C. E. Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol. 1968 Feb 14;31(3):519–540. doi: 10.1016/0022-2836(68)90425-7. [DOI] [PubMed] [Google Scholar]
  9. Cooper S., Ruettinger T. Replication of deoxyribonucleic acid during the division cycle of Salmonella typhimurium. J Bacteriol. 1973 Jun;114(3):966–973. doi: 10.1128/jb.114.3.966-973.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cullum J., Vicente M. Cell growth and length distribution in Escherichia coli. J Bacteriol. 1978 Apr;134(1):330–337. doi: 10.1128/jb.134.1.330-337.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Donachie W. D., Begg K. J. Growth of the bacterial cell. Nature. 1970 Sep 19;227(5264):1220–1224. doi: 10.1038/2271220a0. [DOI] [PubMed] [Google Scholar]
  12. Donachie W. D., Begg K. J., Vicente M. Cell length, cell growth and cell division. Nature. 1976 Nov 25;264(5584):328–333. doi: 10.1038/264328a0. [DOI] [PubMed] [Google Scholar]
  13. Ecker R. E., Kokaisl G. Synthesis of protein, ribonucleic acid, and ribosomes by individual bacterial cells in balanced growth. J Bacteriol. 1969 Jun;98(3):1219–1226. doi: 10.1128/jb.98.3.1219-1226.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Goodell E. W. Recycling of murein by Escherichia coli. J Bacteriol. 1985 Jul;163(1):305–310. doi: 10.1128/jb.163.1.305-310.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Goodell E. W., Schwarz U. Release of cell wall peptides into culture medium by exponentially growing Escherichia coli. J Bacteriol. 1985 Apr;162(1):391–397. doi: 10.1128/jb.162.1.391-397.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grover N. B., Woldringh C. L., Zaritsky A., Rosenberger R. F. Elongation of rod-shaped bacteria. J Theor Biol. 1977 Jul 21;67(2):181–193. doi: 10.1016/0022-5193(77)90192-8. [DOI] [PubMed] [Google Scholar]
  17. HOFFMAN H., FRANK M. E. TIME-LAPSE PHOTOMICROGRAPHY OF CELL GROWTH AND DIVISION IN ESCHERICHIA COLI. J Bacteriol. 1965 Jan;89:212–216. doi: 10.1128/jb.89.1.212-216.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Harvey R. J., Marr A. G., Painter P. R. Kinetics of growth of individual cells of Escherichia coli and Azotobacter agilis. J Bacteriol. 1967 Feb;93(2):605–617. doi: 10.1128/jb.93.2.605-617.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Helmstetter C. E. DNA synthesis during the division cycle of rapidly growing Escherichia coli B/r. J Mol Biol. 1968 Feb 14;31(3):507–518. doi: 10.1016/0022-2836(68)90424-5. [DOI] [PubMed] [Google Scholar]
  20. Hoffmann B., Messer W., Schwarz U. Regulation of polar cap formation in the life cycle of Escherichia coli. J Supramol Struct. 1972;1(1):29–37. doi: 10.1002/jss.400010105. [DOI] [PubMed] [Google Scholar]
  21. KJELDGAARD N. O., MAALOE O., SCHAECHTER M. The transition between different physiological states during balanced growth of Salmonella typhimurium. J Gen Microbiol. 1958 Dec;19(3):607–616. doi: 10.1099/00221287-19-3-607. [DOI] [PubMed] [Google Scholar]
  22. KOCH A. L., LEVY H. R. Protein turnover in growing cultures of Escherichia coli. J Biol Chem. 1955 Dec;217(2):947–957. [PubMed] [Google Scholar]
  23. KOCH A. L., SCHAECHTER M. A model for statistics of the cell division process. J Gen Microbiol. 1962 Nov;29:435–454. doi: 10.1099/00221287-29-3-435. [DOI] [PubMed] [Google Scholar]
  24. Koch A. L., Blumberg G. Distribution of bacteria in the velocity gradient centrifuge. Biophys J. 1976 May;16(5):389–405. doi: 10.1016/S0006-3495(76)85696-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Koch A. L., Burdett I. D. The variable T model for gram-negative morphology. J Gen Microbiol. 1984 Sep;130(9):2325–2338. doi: 10.1099/00221287-130-9-2325. [DOI] [PubMed] [Google Scholar]
  26. Koch A. L. How bacteria grow and divide in spite of internal hydrostatic pressure. Can J Microbiol. 1985 Dec;31(12):1071–1084. doi: 10.1139/m85-204. [DOI] [PubMed] [Google Scholar]
  27. Koch A. L. On the growth and form of Escherichia coli. J Gen Microbiol. 1982 Nov;128(11):2527–2539. doi: 10.1099/00221287-128-11-2527. [DOI] [PubMed] [Google Scholar]
  28. Koch A. L. The surface stress theory of microbial morphogenesis. Adv Microb Physiol. 1983;24:301–366. doi: 10.1016/s0065-2911(08)60388-4. [DOI] [PubMed] [Google Scholar]
  29. Koch A. L., Verwer R. W., Nanninga N. Incorporation of diaminopimelic acid into the old poles of Escherichia coli. J Gen Microbiol. 1982 Dec;128(12):2893–2898. doi: 10.1099/00221287-128-12-2893. [DOI] [PubMed] [Google Scholar]
  30. Koppes L. H., Woldringh C. L., Nanninga N. Size variations and correlation of different cell cycle events in slow-growing Escherichia coli. J Bacteriol. 1978 May;134(2):423–433. doi: 10.1128/jb.134.2.423-433.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Koppes L. J., Nanninga N. Positive correlation between size at initiation of chromosome replication in Escherichia coli and size at initiation of cell constriction. J Bacteriol. 1980 Jul;143(1):89–99. doi: 10.1128/jb.143.1.89-99.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Koppes L. J., Overbeeke N., Nanninga N. DNA replication pattern and cell wall growth in Escherichia coli PAT 84. J Bacteriol. 1978 Mar;133(3):1053–1061. doi: 10.1128/jb.133.3.1053-1061.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kubitschek H. E., Baldwin W. W., Graetzer R. Buoyant density constancy during the cell cycle of Escherichia coli. J Bacteriol. 1983 Sep;155(3):1027–1032. doi: 10.1128/jb.155.3.1027-1032.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kubitschek H. E., Baldwin W. W., Schroeter S. J., Graetzer R. Independence of buoyant cell density and growth rate in Escherichia coli. J Bacteriol. 1984 Apr;158(1):296–299. doi: 10.1128/jb.158.1.296-299.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kubitschek H. E. Bilinear cell growth of Escherichia coli. J Bacteriol. 1981 Nov;148(2):730–733. doi: 10.1128/jb.148.2.730-733.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kubitschek H. E. Evidence for the generality of linear cell growth. J Theor Biol. 1970 Jul;28(1):15–29. doi: 10.1016/0022-5193(70)90061-5. [DOI] [PubMed] [Google Scholar]
  37. Kubitschek H. E. Increase in cell mass during the division cycle of Escherichia coli B/rA. J Bacteriol. 1986 Nov;168(2):613–618. doi: 10.1128/jb.168.2.613-618.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kubitschek H. E., Woldringh C. L. Cell elongation and division probability during the Escherichia coli growth cycle. J Bacteriol. 1983 Mar;153(3):1379–1387. doi: 10.1128/jb.153.3.1379-1387.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lin E. C., Hirota Y., Jacob F. 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. J Bacteriol. 1971 Oct;108(1):375–385. doi: 10.1128/jb.108.1.375-385.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Loeb A., McGrath B. E., Navre J. M., Pierucci O. Cell division during nutritional upshifts of Escherichia coli. J Bacteriol. 1978 Nov;136(2):631–637. doi: 10.1128/jb.136.2.631-637.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Margolis S. G., Cooper S. Simulation of bacterial growth, cell division, and DNA synthesis. Comput Biomed Res. 1971 Aug;4(4):427–443. doi: 10.1016/0010-4809(71)90026-7. [DOI] [PubMed] [Google Scholar]
  42. Marr A. G., Harvey R. J., Trentini W. C. Growth and division of Escherichia coli. J Bacteriol. 1966 Jun;91(6):2388–2389. doi: 10.1128/jb.91.6.2388-2389.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Martínez-Salas E., Martín J. A., Vicente M. Relationship of Escherichia coli density to growth rate and cell age. J Bacteriol. 1981 Jul;147(1):97–100. doi: 10.1128/jb.147.1.97-100.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Meyer M., De Jong M. A., Demets R., Nanninga N. Length growth of two Escherichia coli B/r substrains. J Bacteriol. 1979 Apr;138(1):17–23. doi: 10.1128/jb.138.1.17-23.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Olijhoek A. J., Klencke S., Pas E., Nanninga N., Schwarz U. Volume growth, murein synthesis, and murein cross-linkage during the division cycle of Escherichia coli PA3092. J Bacteriol. 1982 Dec;152(3):1248–1254. doi: 10.1128/jb.152.3.1248-1254.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Pierucci O. Dimensions of Escherichia coli at various growth rates: model for envelope growth. J Bacteriol. 1978 Aug;135(2):559–574. doi: 10.1128/jb.135.2.559-574.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Previc E. P. Biochemical determination of bacterial morphology and the geometry of cell division. J Theor Biol. 1970 Jun;27(3):471–497. doi: 10.1016/s0022-5193(70)80010-8. [DOI] [PubMed] [Google Scholar]
  48. Pritchard R. H. Review lecture on the growth and form of a bacterial cell. Philos Trans R Soc Lond B Biol Sci. 1974 Feb 21;267(886):303–336. doi: 10.1098/rstb.1974.0003. [DOI] [PubMed] [Google Scholar]
  49. Rosenberger R. F., Grover N. B., Zaritsky A., Woldringh C. L. Control of microbial surface-growth by density. Nature. 1978 Jan 19;271(5642):244–245. doi: 10.1038/271244a0. [DOI] [PubMed] [Google Scholar]
  50. Rosenberger R. F., Grover N. B., Zaritsky A., Woldringh C. L. Surface growth in rod-shaped bacteria. J Theor Biol. 1978 Aug 21;73(4):711–721. doi: 10.1016/0022-5193(78)90132-7. [DOI] [PubMed] [Google Scholar]
  51. Ryter A., Hirota Y., Schwarz U. Process of cellular division in Escherichia coli growth pattern of E. coli murein. J Mol Biol. 1973 Jun 25;78(1):185–195. doi: 10.1016/0022-2836(73)90437-3. [DOI] [PubMed] [Google Scholar]
  52. SCHAECHTER M., WILLIAMSON J. P., HOOD J. R., Jr, KOCH A. L. Growth, cell and nuclear divisions in some bacteria. J Gen Microbiol. 1962 Nov;29:421–434. doi: 10.1099/00221287-29-3-421. [DOI] [PubMed] [Google Scholar]
  53. Sargent M. G. Control of cell length in Bacillus subtilis. J Bacteriol. 1975 Jul;123(1):7–19. doi: 10.1128/jb.123.1.7-19.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Sargent M. G. Surface extension and the cell cycle in prokaryotes. Adv Microb Physiol. 1978;18:105–176. doi: 10.1016/s0065-2911(08)60416-6. [DOI] [PubMed] [Google Scholar]
  55. Schwarz U., Ryter A., Rambach A., Hellio R., Hirota Y. Process of cellular division in Escherichia coli: differention of growth zones in the Sacculus. J Mol Biol. 1975 Nov 15;98(4):749–759. doi: 10.1016/s0022-2836(75)80008-8. [DOI] [PubMed] [Google Scholar]
  56. Skarstad K., Steen H. B., Boye E. Escherichia coli DNA distributions measured by flow cytometry and compared with theoretical computer simulations. J Bacteriol. 1985 Aug;163(2):661–668. doi: 10.1128/jb.163.2.661-668.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Trueba F. J., Neijssel O. M., Woldringh C. L. Generality of the growth kinetics of the average individual cell in different bacterial populations. J Bacteriol. 1982 Jun;150(3):1048–1055. doi: 10.1128/jb.150.3.1048-1055.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Trueba F. J., Woldringh C. L. Changes in cell diameter during the division cycle of Escherichia coli. J Bacteriol. 1980 Jun;142(3):869–878. doi: 10.1128/jb.142.3.869-878.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. VAN TUBERGEN R. P., SETLOW R. B. Quantitative radioautographic studies on exponentially growing cultures of Escherichia coli. The distribution of parental DNA, RNA, protein, and cell wall among progeny cells. Biophys J. 1961 Sep;1:589–625. doi: 10.1016/s0006-3495(61)86911-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Verwer R. W., Nanninga N. Pattern of meso-dl-2,6-diaminopimelic acid incorporation during the division cycle of Escherichia coli. J Bacteriol. 1980 Oct;144(1):327–336. doi: 10.1128/jb.144.1.327-336.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Woldringh C. L., Grover N. B., Rosenberger R. F., Zaritsky A. Dimensional rearrangement of rod-shaped bacteria following nutritional shift-up. II. Experiments with Escherichia coli B/r. J Theor Biol. 1980 Oct 7;86(3):441–454. doi: 10.1016/0022-5193(80)90344-6. [DOI] [PubMed] [Google Scholar]
  62. Zaritsky A. On dimensional determination of rod-shaped bacteria. J Theor Biol. 1975 Oct;54(2):243–248. doi: 10.1016/s0022-5193(75)80129-9. [DOI] [PubMed] [Google Scholar]

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