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
. 1996 Jan 9;93(1):336–341. doi: 10.1073/pnas.93.1.336

Control of cell division in Escherichia coli: regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduction.

D M Sitnikov 1, J B Schineller 1, T O Baldwin 1
PMCID: PMC40233  PMID: 8552633

Abstract

The conditioning of culture medium by the production of growth-regulatory substances is a well-established phenomenon with eukaryotic cells. It has recently been shown that many prokaryotes are also capable of modulating growth, and in some cases sensing cell density, by production of extracellular signaling molecules, thereby allowing single celled prokaryotes to function in some respects as multicellular organisms. As Escherichia coli shifts from exponential growth to stationary growth, many changes occur, including cell division leading to formation of short minicells and expression of numerous genes not expressed in exponential phase. An understanding of the coordination between the morphological changes associated with cell division and the physiological and metabolic changes is of fundamental importance to understanding regulation of the prokaryotic cell cycle. The ftsQA genes, which encode functions required for cell division in E. coli, are regulated by promoters P1 and P2, located upstream of the ftsQ gene. The P1 promoter is rpoS-stimulated and the second, P2, is regulated by a member of the LuxR subfamily of transcriptional activators, SdiA, exhibiting features characteristic of an autoinduction (quorum sensing) mechanism. The activity of SdiA is potentiated by N-acyl-homoserine lactones, which are the autoinducers of luciferase synthesis in luminous marine bacteria as well as of pathogenesis functions in several pathogenic bacteria. A compound(s) produced by E. coli itself during growth in Luria Broth stimulates transcription from P2 in an SdiA-dependent process. Another substance(s) enhances transcription of rpoS and (perhaps indirectly) of ftsQA via promoter P1. It appears that this bimodal control mechanism may comprise a fail-safe system, such that transcription of the ftsQA genes may be properly regulated under a variety of different environmental and physiological conditions.

Full text

PDF
336

Selected References

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

  1. Aldea M., Garrido T., Pla J., Vicente M. Division genes in Escherichia coli are expressed coordinately to cell septum requirements by gearbox promoters. EMBO J. 1990 Nov;9(11):3787–3794. doi: 10.1002/j.1460-2075.1990.tb07592.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bainton N. J., Bycroft B. W., Chhabra S. R., Stead P., Gledhill L., Hill P. J., Rees C. E., Winson M. K., Salmond G. P., Stewart G. S. A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia. Gene. 1992 Jul 1;116(1):87–91. doi: 10.1016/0378-1119(92)90633-z. [DOI] [PubMed] [Google Scholar]
  3. Baldwin T. O., Berends T., Bunch T. A., Holzman T. F., Rausch S. K., Shamansky L., Treat M. L., Ziegler M. M. Cloning of the luciferase structural genes from Vibrio harveyi and expression of bioluminescence in Escherichia coli. Biochemistry. 1984 Jul 31;23(16):3663–3667. doi: 10.1021/bi00311a014. [DOI] [PubMed] [Google Scholar]
  4. Bi E. F., Lutkenhaus J. FtsZ ring structure associated with division in Escherichia coli. Nature. 1991 Nov 14;354(6349):161–164. doi: 10.1038/354161a0. [DOI] [PubMed] [Google Scholar]
  5. Bohannon D. E., Connell N., Keener J., Tormo A., Espinosa-Urgel M., Zambrano M. M., Kolter R. Stationary-phase-inducible "gearbox" promoters: differential effects of katF mutations and role of sigma 70. J Bacteriol. 1991 Jul;173(14):4482–4492. doi: 10.1128/jb.173.14.4482-4492.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Borck K., Beggs J. D., Brammar W. J., Hopkins A. S., Murray N. E. The construction in vitro of transducing derivatives of phage lambda. Mol Gen Genet. 1976 Jul 23;146(2):199–207. doi: 10.1007/BF00268089. [DOI] [PubMed] [Google Scholar]
  7. Boyer H. W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969 May 14;41(3):459–472. doi: 10.1016/0022-2836(69)90288-5. [DOI] [PubMed] [Google Scholar]
  8. Cao J. G., Meighen E. A. Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. J Biol Chem. 1989 Dec 25;264(36):21670–21676. [PubMed] [Google Scholar]
  9. Carson M. J., Barondess J., Beckwith J. The FtsQ protein of Escherichia coli: membrane topology, abundance, and cell division phenotypes due to overproduction and insertion mutations. J Bacteriol. 1991 Apr;173(7):2187–2195. doi: 10.1128/jb.173.7.2187-2195.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Connell N., Han Z., Moreno F., Kolter R. An E. coli promoter induced by the cessation of growth. Mol Microbiol. 1987 Sep;1(2):195–201. doi: 10.1111/j.1365-2958.1987.tb00512.x. [DOI] [PubMed] [Google Scholar]
  11. Cubo M. T., Economou A., Murphy G., Johnston A. W., Downie J. A. Molecular characterization and regulation of the rhizosphere-expressed genes rhiABCR that can influence nodulation by Rhizobium leguminosarum biovar viciae. J Bacteriol. 1992 Jun;174(12):4026–4035. doi: 10.1128/jb.174.12.4026-4035.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Devine J. H., Shadel G. S., Baldwin T. O. Identification of the operator of the lux regulon from the Vibrio fischeri strain ATCC7744. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5688–5692. doi: 10.1073/pnas.86.15.5688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dunlap P. V., Kuo A. Cell density-dependent modulation of the Vibrio fischeri luminescence system in the absence of autoinducer and LuxR protein. J Bacteriol. 1992 Apr;174(8):2440–2448. doi: 10.1128/jb.174.8.2440-2448.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eberhard A., Burlingame A. L., Eberhard C., Kenyon G. L., Nealson K. H., Oppenheimer N. J. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry. 1981 Apr 28;20(9):2444–2449. doi: 10.1021/bi00512a013. [DOI] [PubMed] [Google Scholar]
  15. Eberhard A. Inhibition and activation of bacterial luciferase synthesis. J Bacteriol. 1972 Mar;109(3):1101–1105. doi: 10.1128/jb.109.3.1101-1105.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eberhard A., Widrig C. A., McBath P., Schineller J. B. Analogs of the autoinducer of bioluminescence in Vibrio fischeri. Arch Microbiol. 1986 Oct;146(1):35–40. doi: 10.1007/BF00690155. [DOI] [PubMed] [Google Scholar]
  17. Engebrecht J., Nealson K., Silverman M. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell. 1983 Mar;32(3):773–781. doi: 10.1016/0092-8674(83)90063-6. [DOI] [PubMed] [Google Scholar]
  18. Fuqua W. C., Winans S. C. A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite. J Bacteriol. 1994 May;176(10):2796–2806. doi: 10.1128/jb.176.10.2796-2806.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fuqua W. C., Winans S. C., Greenberg E. P. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol. 1994 Jan;176(2):269–275. doi: 10.1128/jb.176.2.269-275.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gambello M. J., Iglewski B. H. Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J Bacteriol. 1991 May;173(9):3000–3009. doi: 10.1128/jb.173.9.3000-3009.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gray K. M., Passador L., Iglewski B. H., Greenberg E. P. Interchangeability and specificity of components from the quorum-sensing regulatory systems of Vibrio fischeri and Pseudomonas aeruginosa. J Bacteriol. 1994 May;176(10):3076–3080. doi: 10.1128/jb.176.10.3076-3080.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Huisman G. W., Kolter R. Sensing starvation: a homoserine lactone--dependent signaling pathway in Escherichia coli. Science. 1994 Jul 22;265(5171):537–539. doi: 10.1126/science.7545940. [DOI] [PubMed] [Google Scholar]
  23. Jones S., Yu B., Bainton N. J., Birdsall M., Bycroft B. W., Chhabra S. R., Cox A. J., Golby P., Reeves P. J., Stephens S. The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J. 1993 Jun;12(6):2477–2482. doi: 10.1002/j.1460-2075.1993.tb05902.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kaplan H. B., Greenberg E. P. Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J Bacteriol. 1985 Sep;163(3):1210–1214. doi: 10.1128/jb.163.3.1210-1214.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kolter R., Siegele D. A., Tormo A. The stationary phase of the bacterial life cycle. Annu Rev Microbiol. 1993;47:855–874. doi: 10.1146/annurev.mi.47.100193.004231. [DOI] [PubMed] [Google Scholar]
  26. Kuo A., Blough N. V., Dunlap P. V. Multiple N-acyl-L-homoserine lactone autoinducers of luminescence in the marine symbiotic bacterium Vibrio fischeri. J Bacteriol. 1994 Dec;176(24):7558–7565. doi: 10.1128/jb.176.24.7558-7565.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lange R., Hengge-Aronis R. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S. J Bacteriol. 1991 Jul;173(14):4474–4481. doi: 10.1128/jb.173.14.4474-4481.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Loewen P. C., von Ossowski I., Switala J., Mulvey M. R. KatF (sigma S) synthesis in Escherichia coli is subject to posttranscriptional regulation. J Bacteriol. 1993 Apr;175(7):2150–2153. doi: 10.1128/jb.175.7.2150-2153.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mulvey M. R., Switala J., Borys A., Loewen P. C. Regulation of transcription of katE and katF in Escherichia coli. J Bacteriol. 1990 Dec;172(12):6713–6720. doi: 10.1128/jb.172.12.6713-6720.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Murray N. E., Brammar W. J., Murray K. Lambdoid phages that simplify the recovery of in vitro recombinants. Mol Gen Genet. 1977 Jan 7;150(1):53–61. doi: 10.1007/BF02425325. [DOI] [PubMed] [Google Scholar]
  31. Nealson K. H., Platt T., Hastings J. W. Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol. 1970 Oct;104(1):313–322. doi: 10.1128/jb.104.1.313-322.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ochsner U. A., Koch A. K., Fiechter A., Reiser J. Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J Bacteriol. 1994 Apr;176(7):2044–2054. doi: 10.1128/jb.176.7.2044-2054.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pearson J. P., Gray K. M., Passador L., Tucker K. D., Eberhard A., Iglewski B. H., Greenberg E. P. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):197–201. doi: 10.1073/pnas.91.1.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pearson J. P., Passador L., Iglewski B. H., Greenberg E. P. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1490–1494. doi: 10.1073/pnas.92.5.1490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Pierson L. S., 3rd, Keppenne V. D., Wood D. W. Phenazine antibiotic biosynthesis in Pseudomonas aureofaciens 30-84 is regulated by PhzR in response to cell density. J Bacteriol. 1994 Jul;176(13):3966–3974. doi: 10.1128/jb.176.13.3966-3974.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Piper K. R., Beck von Bodman S., Farrand S. K. Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature. 1993 Apr 1;362(6419):448–450. doi: 10.1038/362448a0. [DOI] [PubMed] [Google Scholar]
  37. Pirhonen M., Flego D., Heikinheimo R., Palva E. T. A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J. 1993 Jun;12(6):2467–2476. doi: 10.1002/j.1460-2075.1993.tb05901.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Robinson A. C., Kenan D. J., Hatfull G. F., Sullivan N. F., Spiegelberg R., Donachie W. D. DNA sequence and transcriptional organization of essential cell division genes ftsQ and ftsA of Escherichia coli: evidence for overlapping transcriptional units. J Bacteriol. 1984 Nov;160(2):546–555. doi: 10.1128/jb.160.2.546-555.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Shadel G. S., Baldwin T. O. Identification of a distantly located regulatory element in the luxD gene required for negative autoregulation of the Vibrio fischeri luxR gene. J Biol Chem. 1992 Apr 15;267(11):7690–7695. [PubMed] [Google Scholar]
  40. Shadel G. S., Young R., Baldwin T. O. Use of regulated cell lysis in a lethal genetic selection in Escherichia coli: identification of the autoinducer-binding region of the LuxR protein from Vibrio fischeri ATCC 7744. J Bacteriol. 1990 Jul;172(7):3980–3987. doi: 10.1128/jb.172.7.3980-3987.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sharma S., Stark T. F., Beattie W. G., Moses R. E. Multiple control elements for the uvrC gene unit of Escherichia coli. Nucleic Acids Res. 1986 Mar 11;14(5):2301–2318. doi: 10.1093/nar/14.5.2301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Swift S., Winson M. K., Chan P. F., Bainton N. J., Birdsall M., Reeves P. J., Rees C. E., Chhabra S. R., Hill P. J., Throup J. P. A novel strategy for the isolation of luxI homologues: evidence for the widespread distribution of a LuxR:LuxI superfamily in enteric bacteria. Mol Microbiol. 1993 Nov;10(3):511–520. doi: 10.1111/j.1365-2958.1993.tb00923.x. [DOI] [PubMed] [Google Scholar]
  43. Wang H., Gayda R. C. Quantitative determination of FtsA at different growth rates in Escherichia coli using monoclonal antibodies. Mol Microbiol. 1992 Sep;6(17):2517–2524. doi: 10.1111/j.1365-2958.1992.tb01428.x. [DOI] [PubMed] [Google Scholar]
  44. Wang X. D., de Boer P. A., Rothfield L. I. A factor that positively regulates cell division by activating transcription of the major cluster of essential cell division genes of Escherichia coli. EMBO J. 1991 Nov;10(11):3363–3372. doi: 10.1002/j.1460-2075.1991.tb04900.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Ward J. E., Jr, Lutkenhaus J. Overproduction of FtsZ induces minicell formation in E. coli. Cell. 1985 Oct;42(3):941–949. doi: 10.1016/0092-8674(85)90290-9. [DOI] [PubMed] [Google Scholar]
  46. Zhang L., Murphy P. J., Kerr A., Tate M. E. Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones. Nature. 1993 Apr 1;362(6419):446–448. doi: 10.1038/362446a0. [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