1887

Abstract

Spatial regulation of nucleoids and chromosome-partitioning proteins is important for proper chromosome partitioning in . However, the underlying molecular mechanisms are unknown. In the present work, we showed that mutation or chemical perturbation of secretory A (SecA), an ATPase component of the membrane protein translocation machinery, SecY, a component of the membrane protein translocation channel and acyl carrier protein P (AcpP), which binds to SecA and MukB, a functional homologue of structural maintenance of chromosomes protein (SMC), resulted in a defect in chromosome partitioning. We further showed that SecA is essential for proper positioning of the DNA region, decatenation and maintenance of superhelicity of DNA. Genetic interaction studies revealed that the topological abnormality observed in the mutant was due to combined inhibitory effects of defects in MukB, DNA gyrase and Topo IV, suggesting a role for the membrane protein translocation machinery in chromosome partitioning and/or structural maintenance of chromosomes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.077685-0
2014-08-01
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/8/1648.html?itemId=/content/journal/micro/10.1099/mic.0.077685-0&mimeType=html&fmt=ahah

References

  1. Adachi S., Hiraga S.. ( 2003;). Mutants suppressing novobiocin hypersensitivity of a mukB null mutation. . J Bacteriol 185:, 3690–3695. [CrossRef][PubMed]
    [Google Scholar]
  2. Adachi S., Fukushima T., Hiraga S.. ( 2008;). Dynamic events of sister chromosomes in the cell cycle of Escherichia coli.. Genes Cells 13:, 181–197. [CrossRef][PubMed]
    [Google Scholar]
  3. Akiyama Y., Ito K.. ( 1990;). SecY protein, a membrane-embedded secretion factor of E. coli, is cleaved by the ompT protease in vitro.. Biochem Biophys Res Commun 167:, 711–715. [CrossRef][PubMed]
    [Google Scholar]
  4. Appleyard R. K.. ( 1954;). Segregation of new lysogenic types during growth of a doubly lysogenic strain derived from Escherichia coli K12. . Genetics 39:, 440–452.[PubMed]
    [Google Scholar]
  5. Baba T., Jacq A., Brickman E., Beckwith J., Taura T., Ueguchi C., Akiyama Y., Ito K.. ( 1990;). Characterization of cold-sensitive secY mutants of Escherichia coli.. J Bacteriol 172:, 7005–7010.[PubMed]
    [Google Scholar]
  6. Bates D., Kleckner N.. ( 2005;). Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. . Cell 121:, 899–911. [CrossRef][PubMed]
    [Google Scholar]
  7. Butland G., Peregrín-Alvarez J. M., Li J., Yang W., Yang X., Canadien V., Starostine A., Richards D., Beattie B.. & other authors ( 2005;). Interaction network containing conserved and essential protein complexes in Escherichia coli.. Nature 433:, 531–537. [CrossRef][PubMed]
    [Google Scholar]
  8. Carl P. L.. ( 1970;). Escherichia coli mutants with temperature-sensitive synthesis of DNA. . Mol Gen Genet 109:, 107–122. [CrossRef][PubMed]
    [Google Scholar]
  9. Davis T. N., Muller E. D., Cronan J. E. J. Jr. ( 1982;). The virion of the lipid-containing bacteriophage PR4. . Virology 120:, 287–306. [CrossRef][PubMed]
    [Google Scholar]
  10. De Lay N. R., Cronan J. E.. ( 2006;). Gene-specific random mutagenesis of Escherichia coli in vivo: isolation of temperature-sensitive mutations in the acyl carrier protein of fatty acid synthesis. . J Bacteriol 188:, 287–296. [CrossRef][PubMed]
    [Google Scholar]
  11. Fisher J. K., Bourniquel A., Witz G., Weiner B., Prentiss M., Kleckner N.. ( 2013;). Four-dimensional imaging of E. coli nucleoid organization and dynamics in living cells. . Cell 153:, 882–895. [CrossRef][PubMed]
    [Google Scholar]
  12. Hayama R., Marians K. J.. ( 2010;). Physical and functional interaction between the condensin MukB and the decatenase topoisomerase IV in Escherichia coli.. Proc Natl Acad Sci U S A 107:, 18826–18831. [CrossRef][PubMed]
    [Google Scholar]
  13. Hayama R., Bahng S., Karasu M. E., Marians K. J.. ( 2013;). The MukB-ParC interaction affects the intramolecular, not intermolecular, activities of topoisomerase IV. . J Biol Chem 288:, 7653–7661. [CrossRef][PubMed]
    [Google Scholar]
  14. Hill C. W., Harnish B. W.. ( 1981;). Inversions between ribosomal RNA genes of Escherichia coli. . Proc Natl Acad Sci U S A 78:, 7069–7072. [CrossRef][PubMed]
    [Google Scholar]
  15. Hinton J. C. D., Santos D. S., Seirafi A., Hulton C. S. J., Pavitt G. D., Higgins C. F.. ( 1992;). Expression and mutational analysis of the nucleoid-associated protein H-NS of Salmonella typhimurium.. Mol Microbiol 6:, 2327–2337. [CrossRef][PubMed]
    [Google Scholar]
  16. Hiraga S.. ( 2000;). Dynamic localization of bacterial and plasmid chromosomes. . Annu Rev Genet 34:, 21–59. [CrossRef][PubMed]
    [Google Scholar]
  17. Hiraga S., Niki H., Ogura T., Ichinose C., Mori H., Ezaki B., Jaffé A.. ( 1989;). Chromosome partitioning in Escherichia coli: novel mutants producing anucleate cells. . J Bacteriol 171:, 1496–1505.[PubMed]
    [Google Scholar]
  18. Hiraga S., Ichinose C., Niki H., Yamazoe M.. ( 1998;). Cell cycle-dependent duplication and bidirectional migration of SeqA-associated DNA-protein complexes in E. coli.. Mol Cell 1:, 381–387. [CrossRef][PubMed]
    [Google Scholar]
  19. Hiraga S., Ichinose C., Onogi T., Niki H., Yamazoe M.. ( 2000;). Bidirectional migration of SeqA-bound hemimethylated DNA clusters and pairing of oriC copies in Escherichia coli.. Genes Cells 5:, 327–341. [CrossRef][PubMed]
    [Google Scholar]
  20. Ito K., Bassford P. J. Jr, Beckwith J.. ( 1981;). Protein localization in E. coli: is there a common step in the secretion of periplasmic and outer-membrane proteins?. Cell 24:, 707–717. [CrossRef][PubMed]
    [Google Scholar]
  21. Kang S., Han J. S., Park J. H., Skarstad K., Hwang D. S.. ( 2003;). SeqA protein stimulates the relaxing and decatenating activities of topoisomerase IV. . J Biol Chem 278:, 48779–48785. [CrossRef][PubMed]
    [Google Scholar]
  22. Kato J. I., Nishimura Y., Yamada M., Suzuki H., Hirota Y.. ( 1988;). Gene organization in the region containing a new gene involved in chromosome partition in Escherichia coli.. J Bacteriol 170:, 3967–3977.[PubMed]
    [Google Scholar]
  23. Kruse T., Blagoev B., Løbner-Olesen A., Wachi M., Sasaki K., Iwai N., Mann M., Gerdes K.. ( 2006;). Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli.. Genes Dev 20:, 113–124. [CrossRef][PubMed]
    [Google Scholar]
  24. Lau I. F., Filipe S. R., Søballe B., Økstad O.-A., Barre F.-X., Sherratt D. J.. ( 2003;). Spatial and temporal organization of replicating Escherichia coli chromosomes. . Mol Microbiol 49:, 731–743. [CrossRef][PubMed]
    [Google Scholar]
  25. Li Y., Stewart N. K., Berger A. J., Vos S., Schoeffler A. J., Berger J. M., Chait B. T., Oakley M. G.. ( 2010;). Escherichia coli condensin MukB stimulates topoisomerase IV activity by a direct physical interaction. . Proc Natl Acad Sci U S A 107:, 18832–18837. [CrossRef][PubMed]
    [Google Scholar]
  26. Miller J. H.. ( 1992;). New York:: Cold Spring Harbor Laboratory Press;. Minimal Salts: A short course in bacterial genetics.
    [Google Scholar]
  27. Miller A., Wang L., Kendall D. A.. ( 2002;). SecB modulates the nucleotide-bound state of SecA and stimulates ATPase activity. . Biochemistry 41:, 5325–5332. [CrossRef][PubMed]
    [Google Scholar]
  28. Natale P., Swaving J., van der Does C., de Keyzer J., Driessen A. J. M.. ( 2004;). Binding of SecA to the SecYEG complex accelerates the rate of nucleotide exchange on SecA. . J Biol Chem 279:, 13769–13777. [CrossRef][PubMed]
    [Google Scholar]
  29. Niki H., Jaffé A., Imamura R., Ogura T., Hiraga S.. ( 1991;). The new gene mukB codes for a 177kd protein with coiled-coil domains involved in chromosome partitioning of E. coli.. EMBO J 10:, 189–193. [PubMed]
    [Google Scholar]
  30. Niki H., Imamura R., Kitaoka M., Yamanaka K., Ogura T., Hiraga S.. ( 1992;). E.coli MukB protein involved in chromosome partition forms a homodimer with a rod-and-hinge structure having DNA binding and ATP/GTP binding activities. . EMBO J 11:, 5101–5109.[PubMed]
    [Google Scholar]
  31. Nolivos S., Sherratt D.. ( 2014;). The bacterial chromosome: architecture and action of bacterial SMC and SMC-like complexes. . FEMS Microbiol Rev 38:, 380–392. [CrossRef][PubMed]
    [Google Scholar]
  32. Ohsumi K., Yamazoe M., Hiraga S.. ( 2001;). Different localization of SeqA-bound nascent DNA clusters and MukF–MukE–MukB complex in Escherichia coli cells. . Mol Microbiol 40:, 835–845. [CrossRef][PubMed]
    [Google Scholar]
  33. Oliver D. B., Beckwith J.. ( 1981;). E. coli mutant pleiotropically defective in the export of secreted proteins. . Cell 25:, 765–772. [CrossRef][PubMed]
    [Google Scholar]
  34. Oliver D. B., Cabelli R. J., Dolan K. M., Jarosik G. P.. ( 1990;). Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. . Proc Natl Acad Sci U S A 87:, 8227–8231. [CrossRef][PubMed]
    [Google Scholar]
  35. Onogi T., Yamazoe M., Ichinose C., Niki H., Hiraga S.. ( 2000;). Null mutation of the dam or seqA gene suppresses temperature-sensitive lethality but not hypersensitivity to novobiocin of muk null mutants. . J Bacteriol 182:, 5898–5901. [CrossRef][PubMed]
    [Google Scholar]
  36. Onogi T., Ohsumi K., Katayama T., Hiraga S.. ( 2002;). Replication-dependent recruitment of the beta-subunit of DNA polymerase III from cytosolic spaces to replication forks in Escherichia coli.. J Bacteriol 184:, 867–870. [CrossRef][PubMed]
    [Google Scholar]
  37. Robson A., Collinson I.. ( 2006;). The structure of the Sec complex and the problem of protein translocation. . EMBO Rep 7:, 1099–1103. [CrossRef][PubMed]
    [Google Scholar]
  38. Sun Q., Margolin W.. ( 2004;). Effects of perturbing nucleoid structure on nucleoid occlusion-mediated toporegulation of FtsZ ring assembly. . J Bacteriol 186:, 3951–3959. [CrossRef][PubMed]
    [Google Scholar]
  39. Wang J. C.. ( 2002;). Cellular roles of DNA topoisomerases: a molecular perspective. . Nat Rev Mol Cell Biol 3:, 430–440. [CrossRef][PubMed]
    [Google Scholar]
  40. Weitao T., Nordström K., Dasgupta S.. ( 1999;). Mutual suppression of mukB and seqA phenotypes might arise from their opposing influences on the Escherichia coli nucleoid structure. . Mol Microbiol 34:, 157–168. [CrossRef][PubMed]
    [Google Scholar]
  41. Weitao T., Nordström K., Dasgupta S.. ( 2000;). Escherichia coli cell cycle control genes affect chromosome superhelicity. . EMBO Rep 1:, 494–499. [CrossRef][PubMed]
    [Google Scholar]
  42. Yamaichi Y., Niki H.. ( 2004;). migS, a cis-acting site that affects bipolar positioning of oriC on the Escherichia coli chromosome. . EMBO J 23:, 221–233. [CrossRef][PubMed]
    [Google Scholar]
  43. Yamanaka K., Ogura T., Niki H., Hiraga S.. ( 1996;). Identification of two new genes, mukE and mukF, involved in chromosome partitioning in Escherichia coli.. Mol Gen Genet 250:, 241–251.[PubMed]
    [Google Scholar]
  44. Yamazoe M., Adachi S., Kanaya S., Ohsumi K., Hiraga S.. ( 2005;). Sequential binding of SeqA protein to nascent DNA segments at replication forks in synchronized cultures of Escherichia coli.. Mol Microbiol 55:, 289–298. [CrossRef][PubMed]
    [Google Scholar]
  45. Zechiedrich E. L., Cozzarelli N. R.. ( 1995;). Roles of topoisomerase IV and DNA gyrase in DNA unlinking during replication in Escherichia coli.. Genes Dev 9:, 2859–2869. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.077685-0
Loading
/content/journal/micro/10.1099/mic.0.077685-0
Loading

Data & Media loading...

Supplements

Supplementary Material 

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error