Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1982 Dec;152(3):1231–1240. doi: 10.1128/jb.152.3.1231-1240.1982

Cosegregation of cell wall and DNA in Bacillus subtilis.

J M Schlaeppi, D Karamata
PMCID: PMC221630  PMID: 6815164

Abstract

Cosegregation of cell wall and DNA of a lysis-negative mutant of Bacillus subtilis was examined by continuously labeling (i) cell wall, (ii) DNA, and (iii) both cell wall and DNA. After four to five generations of chase in liquid media it was found by light microscope autoradiography that the numbers of wall segregation units per cell are 29 and 9 in rich and minimal medium, respectively. Under the same conditions the numbers of segregation units of DNA were almost 50% lower: 15 and 5, respectively. Simultaneous labeling of cell wall and DNA (iii) provided figures almost identical to those obtained for cell wall alone, (i), implying cosegregation of the two components. Statistical analysis ruled out their random distribution into daughter cells. Measurements of the positions of grain clusters at the end of the chase period along chains of cells, each derived from a single cell at the beginning of chase, show that cell wall units are localized according to a symmetrical pattern, whereas those of DNA are distributed in an asymmetrical but highly regular way. It appears that of two cell wall units of the same age one only has a strand of DNA attached to it. We present a simple diagrammatic model of cell wall organization and DNA-cell wall association which is compatible with our observations. Finally, we discuss previous experiments pertinent to cosegregation of cell wall and DNA obtained with cells grown on solid media as well as with germinating spores; an explanation for the independent segregation of cell wall and DNA observed in the latter case is advanced.

Full text

PDF
1231

Images in this article

1235Image
on p.1235

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Archibald A. R. Cell wall assembly in Bacillus subtilis: development of bacteriophage-binding properties as a result of the pulsed incorporation of teichoic acid. J Bacteriol. 1976 Aug;127(2):956–960. doi: 10.1128/jb.127.2.956-960.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beeson J., Sueoka N. Membrane enrichment of genetic markers close to the origin and terminus during the deoxyribonucleic acid replication cycle in Bacillus subtilis. J Bacteriol. 1979 Sep;139(3):911–916. doi: 10.1128/jb.139.3.911-916.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Briles E. B., Tomasz A. Radioautographic evidence for equatorial wall growth in a gram-positive bacterium. Segregation of choline-3H-labeled teichoic acid. J Cell Biol. 1970 Dec;47(3):786–790. doi: 10.1083/jcb.47.3.786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chai N. C., Lark K. G. Segregation of deoxyribonucleic acid in bacteria: association of the segregating unit with the cell envelope. J Bacteriol. 1967 Aug;94(2):415–421. doi: 10.1128/jb.94.2.415-421.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cole R. M. Symposium on the fine structure and replication of bacteria and their parts. 3. Bacterial cell-wall replication followed by immunofluorescence. Bacteriol Rev. 1965 Sep;29(3):326–344. doi: 10.1128/br.29.3.326-344.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Doyle R. J., Streips U. N., Imada S., Fan V. S., Brown W. C. Genetic transformation with cell wall-associated deoxyribonucleic acid in Bacillus subtilis. J Bacteriol. 1980 Dec;144(3):957–966. doi: 10.1128/jb.144.3.957-966.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. FARMER J. L., ROTHMAN F. TRANSFORMABLE THYMINE-REQUIRING MUTANT OF BACILLUS SUBTILS. J Bacteriol. 1965 Jan;89:262–263. doi: 10.1128/jb.89.1.262-263.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fein J. E., Rogers H. J. Autolytic enzyme-deficient mutants of Bacillus subtilis 168. J Bacteriol. 1976 Sep;127(3):1427–1442. doi: 10.1128/jb.127.3.1427-1442.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Higgins M. L., Shockman G. D. Study of cycle of cell wall assembly in Streptococcus faecalis by three-dimensional reconstructions of thin sections of cells. J Bacteriol. 1976 Sep;127(3):1346–1358. doi: 10.1128/jb.127.3.1346-1358.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hitchins A. D. Patterns of cell polarity and chromosome segregation in chains of sporulating Bacillus megaterium. J Gen Microbiol. 1980 Sep;120(1):51–56. doi: 10.1099/00221287-120-1-51. [DOI] [PubMed] [Google Scholar]
  12. Jacob F., Ryter A., Cuzin F. On the association between DNA and membrane in bacteria. Proc R Soc Lond B Biol Sci. 1966 Mar 22;164(995):267–278. doi: 10.1098/rspb.1966.0029. [DOI] [PubMed] [Google Scholar]
  13. Leibowitz P. J., Schaechter M. The attachment of the bacterial chromosome to the cell membrane. Int Rev Cytol. 1975;41:1–28. doi: 10.1016/s0074-7696(08)60964-x. [DOI] [PubMed] [Google Scholar]
  14. Polley H. M., Schlaeppi J. M., Karamata D. Localised insertion of new cell wall in Bacillus subtilis. Nature. 1978 Jul 20;274(5668):264–266. doi: 10.1038/274264a0. [DOI] [PubMed] [Google Scholar]
  15. Pooley H. M. Layered distribution, according to age, within the cell wall of bacillus subtilis. J Bacteriol. 1976 Mar;125(3):1139–1147. doi: 10.1128/jb.125.3.1139-1147.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pooley H. M. Turnover and spreading of old wall during surface growth of Bacillus subtilis. J Bacteriol. 1976 Mar;125(3):1127–1138. doi: 10.1128/jb.125.3.1127-1138.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Ryter A., Jacob F. Ségrégation des noyaux pendant la croissance et la germination de B. subtilis. C R Acad Sci Hebd Seances Acad Sci D. 1967 May 3;264(18):2254–2256. [PubMed] [Google Scholar]
  19. Schlaeppi J. M., Pooley H. M., Karamata D. Identification of cell wall subunits in bacillus subtilis and analysis of their segregation during growth. J Bacteriol. 1982 Jan;149(1):329–337. doi: 10.1128/jb.149.1.329-337.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Wake R. G. Segregation of Bacillus subtilis chromosomes radioactively labeled during the first round of replication after germination of spores. J Bacteriol. 1976 Jul;127(1):433–439. doi: 10.1128/jb.127.1.433-439.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. YOSHIKAWA H., O'SULLIVAN A., SUEOKA N. SEQUENTIAL REPLICATION OF THE BACILLUS SUBTILIS CHROMOSOME. 3. REGULATION OF INITIATION. Proc Natl Acad Sci U S A. 1964 Oct;52:973–980. doi: 10.1073/pnas.52.4.973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Yoshikawa H. Chromosomes in Bacillus subtilis spores and their segregation during germination. J Bacteriol. 1968 Jun;95(6):2282–2292. doi: 10.1128/jb.95.6.2282-2292.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. de Chastellier C., Hellio R., Ryter A. Study of cell wall growth in Bacillus megaterium by high-resolution autoradiography. J Bacteriol. 1975 Sep;123(3):1184–1196. doi: 10.1128/jb.123.3.1184-1196.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES