Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1974 May;118(2):334–341. doi: 10.1128/jb.118.2.334-341.1974

Electron Microscope and Autoradiographic Study of Ultrastructural Aspects of Competence and Deoxyribonucleic Acid Absorption in Bacillus subtilis: Ultrastructure of Competent and Noncompetent Cells and Cellular Changes During Development of Competence

C A Vermeulen 1, G Venema 2
PMCID: PMC246763  PMID: 4208130

Abstract

By means of electron microscope autoradiography of component cultures of Bacillus subtilis exposed to [3H]thymidine-labeled transforming deoxyribonucleic acid competent and noncompetent cells can be distinguished. Competence is not limited to a specific phase of the cell division cycle. With serial section electron microscopy of competent and noncompetent cells, two types of mesosomal structures are observed: mesosomes connected to the plasma membrane only (plasma membrane mesosomes) and mesosomes which are additionally connected to the nuclear bodies (nuclear mesosomes). The two types show different cellular distributions. Especially the number of nuclear mesosomes is higher in competent than in noncompetent cells. This, and the observation that the increase and decrease of competence is correlated with both the number of cells carrying nuclear mesosomes and the number of nuclear mesosomes per cell, suggests that mesosomes are involved in the acquisition of competence.

Full text

PDF
334

Selected References

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

  1. Akrigg A., Ayad S. R. Studies on the competence-inducing factor of Bacillus subtilis. Biochem J. 1970 Apr;117(2):397–403. doi: 10.1042/bj1170397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bodmer W. F. Recombination and integration in Bacillus subtilis transformation: involvement of DNA synthesis. J Mol Biol. 1965 Dec;14(2):534–557. doi: 10.1016/s0022-2836(65)80203-0. [DOI] [PubMed] [Google Scholar]
  3. Bresler S. E., Kreneva R. A., Kushev V. V. Correction of molecular heterozygotes in the course of transformation. Mol Gen Genet. 1968;102(3):257–268. doi: 10.1007/BF00385983. [DOI] [PubMed] [Google Scholar]
  4. CARO L. G., VAN TUBERGEN R. P., KOLB J. A. High-resolution autoradiography. I. Methods. J Cell Biol. 1962 Nov;15:173–188. doi: 10.1083/jcb.15.2.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cahn F. H., Fox M. S. Fractionation of transformable bacteria from ocompetent cultures of Bacillus subtilis on renografin gradients. J Bacteriol. 1968 Mar;95(3):867–875. doi: 10.1128/jb.95.3.867-875.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dooley D. C., Hadden C. T., Nester E. W. Macromolecular synthesis in Bacillus subtilis during development of the competent state. J Bacteriol. 1971 Nov;108(2):668–679. doi: 10.1128/jb.108.2.668-679.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Epstein H. T. X-ray study of competence development in Bacillus subtilis. Mol Gen Genet. 1971;110(4):327–331. doi: 10.1007/BF00438274. [DOI] [PubMed] [Google Scholar]
  8. Erickson R. J., Copeland J. C. Structure and replication of chromosomes in competent cells of Bacillus subtilis. J Bacteriol. 1972 Mar;109(3):1075–1084. doi: 10.1128/jb.109.3.1075-1084.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ferrandes B., Chaix P., Ryter A. Localisation des cytochromes de Bacillus subtilis dans les structures mésosomiques. C R Acad Sci Hebd Seances Acad Sci D. 1966 Nov 21;263(21):1632–1635. [PubMed] [Google Scholar]
  10. GOODGAL S. H., HERRIOTT R. M. Studies on transformations of Hemophilus influenzae. I. Competence. J Gen Physiol. 1961 Jul;44:1201–1227. doi: 10.1085/jgp.44.6.1201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ghosh B. K., Murray R. G. Fractionation and characterization of the plasma and mesosome membrane of Listeria monocytogenes. J Bacteriol. 1969 Jan;97(1):426–440. doi: 10.1128/jb.97.1.426-440.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hadden C., Nester E. W. Purification of competent cells in the Bacillus subtilis transformation system. J Bacteriol. 1968 Mar;95(3):876–885. doi: 10.1128/jb.95.3.876-885.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Javor G. T., Tomasz A. An autoradiographic study of genetic transformation. Proc Natl Acad Sci U S A. 1968 Aug;60(4):1216–1222. doi: 10.1073/pnas.60.4.1216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. McCarthy C., Nester E. W. Macromolecular synthesis in newly transformed cells of Bacillus subtilis. J Bacteriol. 1967 Jul;94(1):131–140. doi: 10.1128/jb.94.1.131-140.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. NESTER E. W. PENICILLIN RESISTANCE OF COMPETENT CELLS IN DEOXYRIBONUCLEIC ACID TRANSFORMATION OF BACILLUS SUBTILIS. J Bacteriol. 1964 Apr;87:867–875. doi: 10.1128/jb.87.4.867-875.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Patch C. T., Landman O. E. Comparison of the biochemistry and rates of synthesis of mesosomal and peripheral membranes in Bacillus subtilis. J Bacteriol. 1971 Jul;107(1):345–357. doi: 10.1128/jb.107.1.345-357.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Reaveley D. A., Rogers H. J. Some enzymic activities and chemical properties of the mesosomes and cytoplasmic membranes of Bacillus licheniformis 6346. Biochem J. 1969 Jun;113(1):67–79. doi: 10.1042/bj1130067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Sargent M. G., Ghosh B. K., Lampen J. O. Localization of cell-bound penicillinase in Bacillus licheniformis. J Bacteriol. 1968 Oct;96(4):1329–1338. doi: 10.1128/jb.96.4.1329-1338.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sedar A. W., Burde R. M. The demonstration of the succinic dehydrogenase system in Bacillus subtilis using tetranitro--blue tetrazolium combined with techniques of electron microscopy. J Cell Biol. 1965 Oct;27(1):53–66. doi: 10.1083/jcb.27.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Singh R. N., Pitale M. P. Competence and deoxyribonucleic acid uptake in Bacillus subtilis. J Bacteriol. 1968 Mar;95(3):864–866. doi: 10.1128/jb.95.3.864-866.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Smitt W. W., Vermeulen C. A., Vlak J. M., Rozijn T. H., Molenaar I. Electron microscopic autoradiographic study of RNA synthesis in yeast nucleus. Exp Cell Res. 1972 Jan;70(1):140–144. doi: 10.1016/0014-4827(72)90191-7. [DOI] [PubMed] [Google Scholar]
  23. Vermeulen C. A., Venema G. Autoradiographic estimation of competence and the relationship between competence and transformability in cultures of Bacillus subtilis. J Gen Microbiol. 1971 Dec;69(2):239–252. doi: 10.1099/00221287-69-2-239. [DOI] [PubMed] [Google Scholar]
  24. Vermeulen C. A., Venema G. Electron microscope and autoradiographic study of ultrastructural aspects of competence and deoxyribonucleic acid absorption in Bacillus subtilis: localization of uptake and of transport of transforming deoxyribonucleic acid in competent cells. J Bacteriol. 1974 May;118(2):342–350. doi: 10.1128/jb.118.2.342-350.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Vermeulen C. A., Venema G. The effect of competence regime on competence, DNA absorption and integration of DNA in cultures of Bacillus subtilis. J Gen Microbiol. 1972 Aug;71(3):415–424. doi: 10.1099/00221287-71-3-415. [DOI] [PubMed] [Google Scholar]
  26. Wilson G. A., Bott K. F. Nutritional factors influencing the development of competence in the Bacillus subtilis transformation system. J Bacteriol. 1968 Apr;95(4):1439–1449. doi: 10.1128/jb.95.4.1439-1449.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wolstenholme D. R., Vermeulen C. A., Venema G. Evidence for the involvement of membranous bodies in the processes leading to genetic transformation in Bacillus subtilis. J Bacteriol. 1966 Oct;92(4):1111–1121. doi: 10.1128/jb.92.4.1111-1121.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. YOUNG F. E., SPIZIZEN J. BIOCHEMICAL ASPECTS OF COMPETENCE IN THE BACILLUS SUBTILIS TRANSFORMATION SYSTEM. II. AUTOLYTIC ENZYME ACTIVITY OF CELL WALLS. J Biol Chem. 1963 Sep;238:3126–3130. [PubMed] [Google Scholar]
  29. van Iterson W. Symposium on the fine structure and replication of bacteria and their parts. II. Bacterial cytoplasm. Bacteriol Rev. 1965 Sep;29(3):299–325. doi: 10.1128/br.29.3.299-325.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES