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. 1974 May;118(2):681–692. doi: 10.1128/jb.118.2.681-692.1974

Effect of Inhibition of Deoxyribonucleic Acid and Protein Synthesis on the Direction of Cell Wall Growth in Streptococcus faecalis

M L Higgins 1, L Daneo-Moore 1, D Boothby 1, G D Shockman 1
PMCID: PMC246803  PMID: 4133352

Abstract

Selective inhibition of protein synthesis in Streptococcus faecalis (ATCC 9790) was accompanied by a rapid and severe inhibition of cell division and a reduction of enlargement of cellular surface area. Continued synthesis of cell wall polymers resulted in rapid thickening of the wall to an extent not seen in exponential-phase populations. Thus, the normal direction of wall growth was changed from a preferential feeding out of new wall surface to that of thickening existing cell surfaces. However, the overall manner in which the wall thickened, from nascent septa toward polar regions, was the same in both exponential-phase and inhibited populations. In contrast, selective inhibition of deoxyribonucleic acid (DNA) synthesis using mitomycin C was accompanied by an increase in cellular surface area and by division of about 80% of the cells in random populations. Little or no wall thickening was observed until the synthesis of macromolecules other than DNA was impaired and further cell division ceased. Concomitant inhibition of both DNA and protein synthesis inhibited cell division but permitted an increase in average cell volume. In such doubly inhibited cells, walls thickened less than in cells inhibited for protein synthesis only. On the basis of the results obtained, a model for cell surface enlargement and cell division is presented. The model proposes that: (i) each wall enlargement site is influenced by an individual chromosome replication cycle; (ii) during chromosome replication peripheral surface enlargement would be favored over thickening (or septation); (iii) a signal associated with chromosome termination would favor thickening (and septation) at the expense of surface enlargement; and (iv) a factor or signal related to protein synthesis would be required for one or more of the near terminal stages of cell division or cell separation, or both.

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Selected References

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  1. Boothby D., Daneo-Moore L., Higgins M. L., Coyette J., Shockman G. D. Turnover of bacterial cell wall peptidoglycans. J Biol Chem. 1973 Mar 25;248(6):2161–2169. [PubMed] [Google Scholar]
  2. Boothby D., Daneo-Moore L., Shockman G. D. A rapid, guantitative, and selective estimation of radioactively labeled peptidoglycan in gram-positive bacteria. Anal Biochem. 1971 Dec;44(2):645–653. doi: 10.1016/0003-2697(71)90255-7. [DOI] [PubMed] [Google Scholar]
  3. Clark D. J. The regulation of DNA replication and cell division in E. coli B-r. Cold Spring Harb Symp Quant Biol. 1968;33:823–838. doi: 10.1101/sqb.1968.033.01.094. [DOI] [PubMed] [Google Scholar]
  4. Daneo-Moore L., Higgins M. L. Morphokinetic reaction of Streptococcus faecalis (ATCC 9790) cells to the specific inhibition of macromolecular synthesis: nucleoid condensation on the inhibition of protein synthesis. J Bacteriol. 1972 Mar;109(3):1210–1220. doi: 10.1128/jb.109.3.1210-1220.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Giesbrecht P., Ruska H. Uber Veränderungen der Feinstrukturen von Bakterien unter der Einwirkung von Chloramphenicol. Klin Wochenschr. 1968 Jun 1;46(11):575–582. doi: 10.1007/BF01747836. [DOI] [PubMed] [Google Scholar]
  6. Hash J. H., Davies M. C. Electron Microscopy of Staphylococcus aureus Treated with Tetracycline. Science. 1962 Nov 16;138(3542):828–829. doi: 10.1126/science.138.3542.828. [DOI] [PubMed] [Google Scholar]
  7. Heymann H., Manniello J. M., Barkulis S. S. Structure of streptococcal cell walls. V. Phosphate esters in the walls of group A Streptococcus pyogenes. Biochem Biophys Res Commun. 1967 Feb 21;26(4):486–491. doi: 10.1016/0006-291x(67)90574-8. [DOI] [PubMed] [Google Scholar]
  8. Higgins M. L., Daneo-Moore L. Morphokinetic reaction of cells of Streptococcus faecalis (ATCC 9790) to specific inhibition of macromolecular synthesis: dependence of mesosome growth on deoxyribonucleic acid synthesis. J Bacteriol. 1972 Mar;109(3):1221–1231. doi: 10.1128/jb.109.3.1221-1231.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Higgins M. L., Pooley H. M., Shockman G. D. Reinitiation of cell wall growth after threonine starvation of Streptococcus faecalis. J Bacteriol. 1971 Mar;105(3):1175–1183. doi: 10.1128/jb.105.3.1175-1183.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Higgins M. L., Shockman G. D. Early changes in the ultrastructure of Streptococcus faecalis after amino acid starvation. J Bacteriol. 1970 Jul;103(1):244–253. doi: 10.1128/jb.103.1.244-253.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Higgins M. L., Shockman G. D. Model for cell wall growth of Streptococcus faecalis. J Bacteriol. 1970 Feb;101(2):643–648. doi: 10.1128/jb.101.2.643-648.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Higgins M. L., Shockman G. D. Procaryotic cell division with respect to wall and membranes. CRC Crit Rev Microbiol. 1971 May;1(1):29–72. doi: 10.3109/10408417109104477. [DOI] [PubMed] [Google Scholar]
  13. Hirota Y., Ryter A., Jacob F. Thermosensitive mutants of E. coli affected in the processes of DNA synthesis and cellular division. Cold Spring Harb Symp Quant Biol. 1968;33:677–693. doi: 10.1101/sqb.1968.033.01.077. [DOI] [PubMed] [Google Scholar]
  14. Hughes A. H., Stow M., Hancock I. C., Baddiley J. Function of teichoic acids and effect of novobiocin on control of Mg2+ at the bacterial membrane. Nat New Biol. 1971 Jan 13;229(2):53–55. doi: 10.1038/newbio229053a0. [DOI] [PubMed] [Google Scholar]
  15. Hughes R. C., Tanner P. J., Stokes E. Cell-wall thickening in Bacillus subtilis. Comparison of thickened and normal walls. Biochem J. 1970 Nov;120(1):159–170. doi: 10.1042/bj1200159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kubitschek H. E., Freedman M. L. Chromosome replication and the division cycle of Escherichia coli B-r. J Bacteriol. 1971 Jul;107(1):95–99. doi: 10.1128/jb.107.1.95-99.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mauck J., Glaser L. On the mode of in vivo assembly of the cell wall of Bacillus subtilis. J Biol Chem. 1972 Feb 25;247(4):1180–1187. [PubMed] [Google Scholar]
  18. Osborn M. J. Structure and biosynthesis of the bacterial cell wall. Annu Rev Biochem. 1969;38:501–538. doi: 10.1146/annurev.bi.38.070169.002441. [DOI] [PubMed] [Google Scholar]
  19. Painter P. R., Marr A. G. Mathematics of microbial populations. Annu Rev Microbiol. 1968;22:519–548. doi: 10.1146/annurev.mi.22.100168.002511. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Pritchard R. H., Zaritsky A. Effect of thymine concentration on the replication velocity of DNA in a thymineless mutant of Escherichia coli. Nature. 1970 Apr 11;226(5241):126–131. doi: 10.1038/226126a0. [DOI] [PubMed] [Google Scholar]
  22. Reeve J. N., Groves D. J., Clark D. J. Regulation of Cell Division in Escherichia coli: Characterization of Temperature-Sensitive Division Mutants. J Bacteriol. 1970 Dec;104(3):1052–1064. doi: 10.1128/jb.104.3.1052-1064.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rogers H. J. Bacterial growth and the cell envelope. Bacteriol Rev. 1970 Jun;34(2):194–214. doi: 10.1128/br.34.2.194-214.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Roth G. S., Shockman G. D., Daneo-Moore L. Balanced macromolecular biosynthesis in "protoplasts" of Streptococcus faecalis. J Bacteriol. 1971 Mar;105(3):710–717. doi: 10.1128/jb.105.3.710-717.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sayare M., Daneo-Moore L., Shockman G. D. Influence of macromolecular biosynthesis on cellular autolysis in Streptococcus faecalis. J Bacteriol. 1972 Oct;112(1):337–344. doi: 10.1128/jb.112.1.337-344.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shockman G. D. Symposium on the fine structure and replication of bacteria and their parts. IV. Unbalanced cell-wall synthesis: autolysis and cell-wall thickening. Bacteriol Rev. 1965 Sep;29(3):345–358. doi: 10.1128/br.29.3.345-358.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Spratt B. G., Rowbury R. J. Cell division in a mutant of Salmonella typhimurium which is temperature-sensitive for DNA synthesis. J Gen Microbiol. 1971 Mar;65(3):305–314. doi: 10.1099/00221287-65-3-305. [DOI] [PubMed] [Google Scholar]
  28. Thompson J. S. Role of autolytic enzymes in the growth and morphogenesis of bacterial cell walls. J Theor Biol. 1971 Oct;33(1):63–75. doi: 10.1016/0022-5193(71)90216-5. [DOI] [PubMed] [Google Scholar]
  29. Zusman D. R., Inouye M., Pardee A. B. Cell division in Escherichia coli: evidence for regulation of septation by effector molecules. J Mol Biol. 1972 Aug 14;69(1):119–136. doi: 10.1016/0022-2836(72)90027-7. [DOI] [PubMed] [Google Scholar]

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