Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Sep 12;92(19):8630–8634. doi: 10.1073/pnas.92.19.8630

Postseptational chromosome partitioning in bacteria.

M E Sharpe 1, J Errington 1
PMCID: PMC41020  PMID: 7567988

Abstract

Mutations in the spoIIIE gene prevent proper partitioning of one chromosome into the developing prespore during sporulation but have no overt effect on partitioning in vegetatively dividing cells. However, the expression of spoIIIE in vegetative cells and the occurrence of genes closely related to spoIIIE in a range of nonsporulating eubacteria suggested a more general function for the protein. Here we show that SpoIIIE protein is needed for optimal chromosome partitioning in vegetative cells of Bacillus subtilis when the normal tight coordination between septation and nucleoid partitioning is perturbed or when septum positioning is altered. A functional SpoIIIE protein allows cells to recover from a state in which their chromosome has been trapped by a closing septum. By analogy to its function during sporulation, we suggest that SpoIIIE facilitates partitioning by actively translocating the chromosome out of the septum. In addition to enhancing the fidelity of nucleoid partitioning, SpoIIIE also seems to be required for maximal resistance to antibiotics that interfere with DNA metabolism. The results have important implications for our understanding of the functions of genes involved in the primary partitioning machinery in bacteria and of how septum placement is controlled.

Full text

PDF
8631

Images in this article

Selected References

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

  1. Akerlund T., Bernander R., Nordström K. Cell division in Escherichia coli minB mutants. Mol Microbiol. 1992 Aug;6(15):2073–2083. doi: 10.1111/j.1365-2958.1992.tb01380.x. [DOI] [PubMed] [Google Scholar]
  2. Anagnostopoulos C., Spizizen J. REQUIREMENTS FOR TRANSFORMATION IN BACILLUS SUBTILIS. J Bacteriol. 1961 May;81(5):741–746. doi: 10.1128/jb.81.5.741-746.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beall B., Lutkenhaus J. Impaired cell division and sporulation of a Bacillus subtilis strain with the ftsA gene deleted. J Bacteriol. 1992 Apr;174(7):2398–2403. doi: 10.1128/jb.174.7.2398-2403.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown N. C. 6-(p-hydroxyphenylazo)-uracil: a selective inhibitor of host DNA replication in phage-infected Bacillus subtilis. Proc Natl Acad Sci U S A. 1970 Nov;67(3):1454–1461. doi: 10.1073/pnas.67.3.1454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bylund J. E., Haines M. A., Piggot P. J., Higgins M. L. Axial filament formation in Bacillus subtilis: induction of nucleoids of increasing length after addition of chloramphenicol to exponential-phase cultures approaching stationary phase. J Bacteriol. 1993 Apr;175(7):1886–1890. doi: 10.1128/jb.175.7.1886-1890.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Donachie W. D., Martin D. T., Begg K. J. Independence of cell division and DNA replication in Bacillus subtilis. Nat New Biol. 1971 Jun 30;231(26):274–276. doi: 10.1038/newbio231274a0. [DOI] [PubMed] [Google Scholar]
  7. Errington J., Mandelstam J. Use of a lacZ gene fusion to determine the dependence pattern of sporulation operon spoIIA in spo mutants of Bacillus subtilis. J Gen Microbiol. 1986 Nov;132(11):2967–2976. doi: 10.1099/00221287-132-11-2967. [DOI] [PubMed] [Google Scholar]
  8. Foulger D., Errington J. The role of the sporulation gene spoIIIE in the regulation of prespore-specific gene expression in Bacillus subtilis. Mol Microbiol. 1989 Sep;3(9):1247–1255. doi: 10.1111/j.1365-2958.1989.tb00275.x. [DOI] [PubMed] [Google Scholar]
  9. Hauser P. M., Errington J. Characterization of cell cycle events during the onset of sporulation in Bacillus subtilis. J Bacteriol. 1995 Jul;177(14):3923–3931. doi: 10.1128/jb.177.14.3923-3931.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hiraga S. Chromosome and plasmid partition in Escherichia coli. Annu Rev Biochem. 1992;61:283–306. doi: 10.1146/annurev.bi.61.070192.001435. [DOI] [PubMed] [Google Scholar]
  11. Hiraga S., Niki H., Ogura T., Ichinose C., Mori H., Ezaki B., Jaffé A. Chromosome partitioning in Escherichia coli: novel mutants producing anucleate cells. J Bacteriol. 1989 Mar;171(3):1496–1505. doi: 10.1128/jb.171.3.1496-1505.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ireton K., Gunther N. W., 4th, Grossman A. D. spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol. 1994 Sep;176(17):5320–5329. doi: 10.1128/jb.176.17.5320-5329.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lee S., Price C. W. The minCD locus of Bacillus subtilis lacks the minE determinant that provides topological specificity to cell division. Mol Microbiol. 1993 Feb;7(4):601–610. doi: 10.1111/j.1365-2958.1993.tb01151.x. [DOI] [PubMed] [Google Scholar]
  14. Levin P. A., Losick R. Characterization of a cell division gene from Bacillus subtilis that is required for vegetative and sporulation septum formation. J Bacteriol. 1994 Mar;176(5):1451–1459. doi: 10.1128/jb.176.5.1451-1459.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Levin P. A., Margolis P. S., Setlow P., Losick R., Sun D. Identification of Bacillus subtilis genes for septum placement and shape determination. J Bacteriol. 1992 Nov;174(21):6717–6728. doi: 10.1128/jb.174.21.6717-6728.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. McGinness T., Wake R. G. Division septation in the absence of chromosome termination in Bacillus subtilis. J Mol Biol. 1979 Oct 25;134(2):251–264. doi: 10.1016/0022-2836(79)90035-4. [DOI] [PubMed] [Google Scholar]
  17. Miller S., Pesci E. C., Pickett C. L. Genetic organization of the region upstream from the Campylobacter jejuni flagellar gene flhA. Gene. 1994 Aug 19;146(1):31–38. doi: 10.1016/0378-1119(94)90830-3. [DOI] [PubMed] [Google Scholar]
  18. Motallebi-Veshareh M., Rouch D. A., Thomas C. M. A family of ATPases involved in active partitioning of diverse bacterial plasmids. Mol Microbiol. 1990 Sep;4(9):1455–1463. doi: 10.1111/j.1365-2958.1990.tb02056.x. [DOI] [PubMed] [Google Scholar]
  19. Mulder E., Woldringh C. L. Actively replicating nucleoids influence positioning of division sites in Escherichia coli filaments forming cells lacking DNA. J Bacteriol. 1989 Aug;171(8):4303–4314. doi: 10.1128/jb.171.8.4303-4314.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Niki H., Jaffé A., Imamura R., Ogura T., Hiraga S. The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J. 1991 Jan;10(1):183–193. doi: 10.1002/j.1460-2075.1991.tb07935.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Oswald W., Thiele D. A sporulation gene in Coxiella burnetii? Zentralbl Veterinarmed B. 1993 Jul;40(5):366–370. doi: 10.1111/j.1439-0450.1993.tb00151.x. [DOI] [PubMed] [Google Scholar]
  22. Reeve J. N., Mendelson N. H., Coyne S. I., Hallock L. L., Cole R. M. Minicells of Bacillus subtilis. J Bacteriol. 1973 May;114(2):860–873. doi: 10.1128/jb.114.2.860-873.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Varley A. W., Stewart G. C. The divIVB region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (minCD) and cell shape (mreBCD) determinants. J Bacteriol. 1992 Nov;174(21):6729–6742. doi: 10.1128/jb.174.21.6729-6742.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Woldringh C. L., Mulder E., Huls P. G., Vischer N. Toporegulation of bacterial division according to the nucleoid occlusion model. Res Microbiol. 1991 Feb-Apr;142(2-3):309–320. doi: 10.1016/0923-2508(91)90046-d. [DOI] [PubMed] [Google Scholar]
  25. Wu L. J., Errington J. Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science. 1994 Apr 22;264(5158):572–575. doi: 10.1126/science.8160014. [DOI] [PubMed] [Google Scholar]
  26. Wu L. J., Lewis P. J., Allmansberger R., Hauser P. M., Errington J. A conjugation-like mechanism for prespore chromosome partitioning during sporulation in Bacillus subtilis. Genes Dev. 1995 Jun 1;9(11):1316–1326. doi: 10.1101/gad.9.11.1316. [DOI] [PubMed] [Google Scholar]
  27. Yanouri A., Daniel R. A., Errington J., Buchanan C. E. Cloning and sequencing of the cell division gene pbpB, which encodes penicillin-binding protein 2B in Bacillus subtilis. J Bacteriol. 1993 Dec;175(23):7604–7616. doi: 10.1128/jb.175.23.7604-7616.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. de Boer P. A., Crossley R. E., Rothfield L. I. Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J Bacteriol. 1992 Jan;174(1):63–70. doi: 10.1128/jb.174.1.63-70.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. van Helvoort J. M., Woldringh C. L. Nucleoid partitioning in Escherichia coli during steady-state growth and upon recovery from chloramphenicol treatment. Mol Microbiol. 1994 Aug;13(4):577–583. doi: 10.1111/j.1365-2958.1994.tb00452.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES