Molecular and General Genetics MGG

, Volume 205, Issue 1, pp 134–145

A new cell division operon inEscherichia coli

  • Deborah R. Gill
  • Graham F. Hatfull
  • George P. C. Salmond


At 76 min on theE. coli genetic map there is a cluster of genes affecting essential cellular functions, including the heat shock response and cell division. A combination ofin-vivo andin-vitro genetic analysis of cell division mutants suggests that the cell division genefts E is the second gene in a 3 gene operon. A cold-sensitive mutant, defective in the third gene, is also unable to divide at the restrictive temperature, and we designate this new cell division genefts X. Another cell division gene,fts S, is very close to, but distinct from, the 3 genes of the operon. Thefts E product is a 24.5 Kd polypeptide which shows strong homology with a small group of proteins involved in transport. Both thefts E product and the protein coded by the first gene (fts Y) in the operon have a sequence motif found in a wide range of heterogeneous proteins, including the Ras proteins of yeast. This common domain is indicative of a nucleotide-binding site.

Key words

Cell division ftsOperon Nucleotidebinding Transport 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Akiyoshi DE, Regier DA, Jen G, Gordon MP (1985) Cloning and nucleotide sequence of thetzs gene ofAgrobacterium tumefaciens strain T3. Nucleic Acids Res 13:2773–2788PubMedGoogle Scholar
  2. Aksoy S, Squires CL, Squires C (1984) Translational coupling of thetrpB andtrpA genes in theEscherichia coli tryptophan operon. J Bacteriol 157:363–367PubMedGoogle Scholar
  3. Amemura M, Makino K, Shinagawa H, Kobayashi A, Nakata A (1985) Nucleotide sequence of the genes involved in phosphate transport and regulation of the phosphate regulon inEscherichia coli. J Mol Biol 184:241–250PubMedCrossRefGoogle Scholar
  4. Amzel LM, Pedersen PL (1983) Proton ATPases: Structure and mechanism. Ann Rev Biochem 52:801–824PubMedCrossRefGoogle Scholar
  5. Argos P, Kamer G, Nicklin MJH, Wimmer E (1984) Similarity in gene organization and homology between proteins of animal picornaviruses and a plant comovirus suggest common ancestry of these virus families. Nucleic Acids Res 12:7251–7267PubMedGoogle Scholar
  6. Bachmann B (1983) Linkage map ofEscherichia coli K12, edition 7. Microbiol Rev 47:180–230PubMedGoogle Scholar
  7. Band L, Shimotsu H, Henner DJ (1984) Nucleotide sequence of theBacillus subtilis trpE andtrpD genes. Gene 27:55–65PubMedCrossRefGoogle Scholar
  8. Bankier AT, Barrell BG (1983) Shotgun DNA sequencing. In: Techniques in the life sciences, vol B5, Flavell RA (ed). Elsevier Scientific Publishers, Ireland, pp 1–36Google Scholar
  9. Beckner SK, Hattori S, Shih TY (1985) Theras oncogene product p21 is not a regulatory component of adenylate cyclase. Nature 317:71–72PubMedCrossRefGoogle Scholar
  10. Biggin MD, Gibson TJ, Hong GF (1983) Buffer gradient gels and35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci USA 80:3963–3965PubMedCrossRefGoogle Scholar
  11. Bos JL, Toksoz D, Marshall CJ, Verlaan-de Vries M, Veeneman GH, van der Eb AJ, van Boom JH, Janssen JWG Steenvoorden ACH (1985) Amino-acid substitutions at codon 13 of the N-ras oncogene in human acute myeloid leukaemia. Nature 315:726–730PubMedCrossRefGoogle Scholar
  12. Bradshaw HD, Deininger PL (1984) Human thymidine kinase gene: Molecular cloning and nucleotide sequence of a cDNA expressible in mammalian cells. Mol Cell Biol 4:2316–2320PubMedGoogle Scholar
  13. Broek D, Samiy N, Fasano O, Fujiyama A, Tamanoi F, Northup J, Wigler M (1985) Differential activation of yeast adenylate cyclase by wild-type and mutant Ras proteins. Cell 41:763–769PubMedCrossRefGoogle Scholar
  14. Chipperfield RG, Jones SS, Lo K-M, Weinberg RA (1985) Activation of Ha-ras p21 by substitution, deletion and insertion mutations. Mol Cell Biol 5: 1809–1813PubMedGoogle Scholar
  15. Clertlant P, Seif I (1984) A common function for polyoma virus large-T and papillomavirus E1 proteins? Nature 311: 276–279CrossRefGoogle Scholar
  16. Clewell DB, Helinski DR (1970) Properties of a super-coiled deoxyribonucleic acid-protein relaxation complex and strand specificity of the relaxation event. Biochemistry 9: 4428–4440PubMedCrossRefGoogle Scholar
  17. Csonka LN, Clarke AJ (1980) Construction of an Hfr strain useful for transferringrecA mutations betweenE. coli strains. J Bacteriol 143: 529–530PubMedGoogle Scholar
  18. Dassa E, Hofnung M (1985) Sequence of genemalG inE. coli K12: Homologies between integral membrane components from binding protein-dependent transport systems. EMBO J 4: 2287–2293PubMedGoogle Scholar
  19. Debouck C, Riccio A, Schumperli D, McKenney K, Jeffers J, Hughes C, Rosenberg M (1985) Structure of the galactokinase gene ofE. coli, the last (?) gene of thegal operon. Nucleic Acids Res 13: 1841–1852PubMedGoogle Scholar
  20. Deininger PL (1983) Random subcloning of sonicated DNA: Application to shotgun DNA sequence analysis Anal Biochem 129: 216–223PubMedCrossRefGoogle Scholar
  21. Donachie WD, Begg KJ, Sullivan NF (1984) Morphogenes ofE. coli. In: Microbial development, Losick R, Shapiro L (eds) Cold Spring Harbor Laboratory, pp 27–62Google Scholar
  22. Doolittle RF (1981) Similar amino acid sequences: Change or common ancestry. Science 214: 149–159PubMedGoogle Scholar
  23. Dretzen G, Bellard M, Sassone-Corsi P, Chambon P (1981) A reliable method for the recovery of DNA fragments from agarose and acrylamide gels. Anal Biochem 112: 295–298PubMedCrossRefGoogle Scholar
  24. Fasano O, Aldrich T, Tamanoi F, Taparowsky E, Furth M, Wigler M (1984) Analysis of the transforming potential of the human H-ras gene by random mutagenesis Proc Natl Acad Sci USA 81: 4002–4012CrossRefGoogle Scholar
  25. Finch PW, Emmerson PT (1984) The nucleotide sequence of theuvrD gene ofE. coli. Nucl Acids Res 12: 5789–5799PubMedGoogle Scholar
  26. Gay NJ, Walker JE (1983) Homology between human bladder carcinoma oncogene product and mitochondrial ATP-synthase. Nature 301: 262–264PubMedCrossRefGoogle Scholar
  27. Gilson E, Higgins CF, Hofnung M, Ames GF-L, Nakaido H (1982) Extensive homology between membrane associated components of histidine and maltose transport systems ofSalmonella typhimurium andE. coli. J Biol Chem 257: 9915–9918PubMedGoogle Scholar
  28. Guyer MS (1978) The γδ sequence of F is an insertion sequence. J Mol Biol 126: 347–365PubMedCrossRefGoogle Scholar
  29. Haseloff J, Goelet P, Zimmern D, Ahlquist P, Dasgupta R, Kaesberg P (1984) Striking similarities in amino acid sequence among non-structural proteins encoded by RNA viruses that have dissimilar genomic organisations. Proc Natl Acad Sci USA 81: 4358–4362PubMedCrossRefGoogle Scholar
  30. Hearst JE, Alberti M, Doolittle RF (1985) A putative nitrogenase reductase gene found in the nucleotide sequences from the photosynthetic gene cluster ofRhodopseudomonas capsulata. Cell 40: 219–220PubMedCrossRefGoogle Scholar
  31. Helmstetter CE, Pierucci O, Weinberger M, Holmes M, Tang W (1979) Control of cell division inE. coli. In: The Bacteria, vol VII, Sokatch JR, Ornsten LN (eds). Academic Press, London and New York, pp 517–579Google Scholar
  32. Higgins CF, Haag PD, Nikaido K, Ardeshir F, Garcia G, Ames GF-L (1982) Complete nucleotide sequence and identification of membrane components of the histidine transport operon ofS. typhimurium. Nature 298: 723–727PubMedCrossRefGoogle Scholar
  33. Higgins CF, Hiles ID, Whalley K, Jamieson DJ (1985) Nucleotide binding by membrane components of bacterial periplasmic binding protein-dependent transport systems. EMBO J 4: 1033–1040PubMedGoogle Scholar
  34. Hirota Y, Ryter A, Jacob F (1968) Thermosensitive mutants ofE. coli affected in the process of DNA synthesis and cellular division. Cold Spring Harbor Symp Quant Biol 33: 677–693PubMedGoogle Scholar
  35. Hobson A, Weatherwax R, Ames GF-L (1984) ATP-binding sites in the membrane components of histidine permease, a periplasmic transport system. Proc Natl Acad Sci USA 81: 733–7337CrossRefGoogle Scholar
  36. Holland IB, Jones C (1985) The role of the FtsZ protein (sfiB) in UV-induced division inhibition and in the normalE. coli cell division cycle. Ann Inst Pasteur/Microbiol 136: A165–171Google Scholar
  37. Howe CJ, Fearnley IM, Walker JE, Dyer TA, Gray JC (1985) Nucleotide sequences of the genes for the alpha, beta and epsilon chloroplast ATP synthase. Plant Mol Biol 4: 333–346CrossRefGoogle Scholar
  38. Hurley JB, Simon MI, Teplow DB, Robishaw JD, Gilman AG (1984) Homologies between signal transducing G proteins andras gene products. Science 226: 860–862PubMedGoogle Scholar
  39. Jones CA, Holland IB (1984) Inactivation of essential division genes,ftsA,ftsZ suppresses mutations ofsfiB, a locus mediating division inhibition during the SOS response inE. coli. EMBO J 3: 1181–1186PubMedGoogle Scholar
  40. Kataoka T, Powers S, Cameron S, Fasano O, Goldfarb M, Broach J, Wigler M (1985) Functional homology of mammalian and yeast Ras genes. Cell 40: 19–26PubMedCrossRefGoogle Scholar
  41. Kitagawa Y, Akaboshi E, Shinagawa H, Horii T, Ogawa H, Kato T (1985) Structural analysis of theumu operon required for inducible mutagenesis inE. coli. Proc Natl Acad Sci USA 82: 4336–4340PubMedCrossRefGoogle Scholar
  42. Krebbers ET, Larrima IM, McIntosh L, Bogorad L (1982) The maize chloroplast genes for the β and ε subunits of the photosynthetic coupling factor CF1 are defined. Nucl Acids Res 10: 4985–5002PubMedGoogle Scholar
  43. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227: 680–685PubMedCrossRefGoogle Scholar
  44. Little JW, Mount DW (1982) The SOS-regulatory system ofE. coli. Cell 21: 11–22CrossRefGoogle Scholar
  45. Lutkenhaus JF, Donachie WD (1979) Identification of theftsA gene product. J Bacteriol 137: 1088–1094PubMedGoogle Scholar
  46. Madaule P, Axel R (1985) A novelras-related gene family. Cell 41: 31–40PubMedCrossRefGoogle Scholar
  47. Makino K, Shinagawa H, Nakata A (1985) Regulation of the phosphate regulon ofE. coli K-12: regulation and role of the regulatory genephoR. J Mol Biol 184: 231–240PubMedCrossRefGoogle Scholar
  48. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning-a laboratory manual. Cold Spring Harbour LaboratoryGoogle Scholar
  49. Manne V, Bekesi E, Kung H-F (1985) Ha-ras proteins exhibit GTPase activity: point mutations that activate Ha-ras gene products results in decreased GTPase activity. Proc Natl Acad Sci USA 82: 376–380PubMedCrossRefGoogle Scholar
  50. McGrath JP, Capon DJ, Goeddel DV, Levinson AD (1984) Comparative biochemical properties of normal and activated humanras p21 protein. Nature 310: 644–649PubMedCrossRefGoogle Scholar
  51. Messing J, Vieira J (1982) A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene 19: 269–276PubMedCrossRefGoogle Scholar
  52. Moller W, Amons R (1985) Phosphate-binding sequences in nucleotide-binding proteins. FEBS Lett 186: 1–7PubMedCrossRefGoogle Scholar
  53. Ohlendorf DH, Matthews BW (1983) Structural studies of protein nucleic acid interactions. Ann Rev Biophys Bioeng 12: 259–284CrossRefGoogle Scholar
  54. Oppenheim DS, Yanofsky C (1980) Translational coupling during expression of the tryptophan operon ofE. coli. Genetics 95: 785–795PubMedGoogle Scholar
  55. Pabo CO, Sauer RT (1984) Protein-DNA recognition. Ann Rev Biochem 3: 293–321CrossRefGoogle Scholar
  56. Perry KL, Elledge SJ, Mitchell BB, Marsh L, Walker GC (1985)umuDC andmucAB operons whose products are required for UV light- and chemical-induced mutagenesis: UmuD, MucA, and LexA proteins share homology. Proc Natl Acad Sci USA 82: 4331–4335PubMedCrossRefGoogle Scholar
  57. Pincus MR, Brandt-Rauf PW (1985) Structural effects of substitutions on the p21 proteins. Proc Natl Acad Sci USA 82: 3596–3600PubMedCrossRefGoogle Scholar
  58. Plakidou S, Moffat DG, Salmond GPC, Mackinnon G (1984) Convenient transduction ofrecA with bacteriophage T4GT7. J Bacteriol 159: 1072–1073PubMedGoogle Scholar
  59. Powers S, Kataoka T, Fasano O, Goldfarb M, Strathern J, Broach J, Wigler M (1984) Genes inSaccharomyes cerevisiae encoding proteins with domains homologous to the mammalianras proteins. Cell 36: 607–612PubMedCrossRefGoogle Scholar
  60. Reymond CD, Gomer RH, Mehdv MC, Firtel RA (1984) Developmental regulation of aDictyostelium gene encoding a protein homologous to mammalianras protein. Cell 39: 141–148PubMedCrossRefGoogle Scholar
  61. Ricard M, Hirota Y (1973) Process of cellular division inE. coli: Physiological study on thermosensitive mutants defective in cell division. J Bacteriol 116: 314–322PubMedGoogle Scholar
  62. Robinson AC, Kenan DJ, Hatfull GF, Sullivan NF, Spiegelberg R, Donachie WD (1984) DNA sequence and transcriptional organization of essential cell division genesftsQ andftsA ofEscherichia coli: Evidence for overlapping transcriptional units. J Bacteriol 160: 546–555PubMedGoogle Scholar
  63. Sancar A, Hack AM, Rupp WD (1979) Simple method for identification of plasmid coded proteins. J Bacteriol 137: 692–693PubMedGoogle Scholar
  64. Salmond GPC, Plakidou S (1984) Genetic analysis of essential genes in theftsE region of theEscherichia coli genetic map and identification of a new cell division geneftsS. Mol Gen Genet 197: 304–308PubMedCrossRefGoogle Scholar
  65. Schejter ED, Shilo B-Z (1985) Characterization of functional domains of p21ras by use of chimeric genes. EMBO J 4: 407–412PubMedGoogle Scholar
  66. Seeburg PH, Colby WW, Capon DJ, Goeddel DV, Levinson AD (1984) Biological properties of human c-Ha-ras 1 genes mutated at codon 12. Nature 312: 71–75PubMedCrossRefGoogle Scholar
  67. Shinozaki K, Deno H, Kato H, Sugiura M (1983) Overlap and cotranscription of the genes for the β and ε subunits of tobacco chloroplast ATPase. Genet 24: 147–155Google Scholar
  68. Shuman HA, Silhavy TJ (1981) Identification of themalK gene product. J Biol Chem 256: 560–562PubMedGoogle Scholar
  69. Staden R (1982a) An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Res 10: 2951–2961PubMedGoogle Scholar
  70. Staden R (1982b) Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Res 10: 4731–4751PubMedGoogle Scholar
  71. Staden R (1984) Graphic methods to determine the function of nucleic acid sequences. Nucleic Acids Res 12: 521–538PubMedGoogle Scholar
  72. Stanway G, Hughes PJ, Mountford RC, Minor PD, Almond JW (1984) A complete nucleotide sequence of a common cold virus: Human rhinovirus 14. Nucleic Acids Res 12: 7859–7875PubMedGoogle Scholar
  73. Strauss EG, Rice CM, Strauss JH (1984) Complete nucleotide sequence of the genomic RNA of sindbis virus. Virology 133: 92–110PubMedCrossRefGoogle Scholar
  74. Sullivan NF, Donachie WD (1984) Overlapping functional units in a cell division gene cluster inE. coli. J Bacteriol 158: 1198–1201PubMedGoogle Scholar
  75. Surin BP, Rosenberg H, Cox GB (1985) Phosphate-specific transport system ofE. coli: Nucleotide sequence and gene-polypeptide relationships. J Bacteriol 161: 189–198PubMedGoogle Scholar
  76. Tanabe T, Nukada T, Nishikawa Y, Sugimoto K, Suzuki H, Takahashi H, Noda M, Haga T, Ichiyama A, Kanagawa K Minamino N, Matsuo H, Numa S (1985) Primary structure of the α-subunit of transducin and its relationship toras protein. Nature 315: 242–245PubMedCrossRefGoogle Scholar
  77. Taya Y, Hosogai K, Hirohashi S, Shimosato Y, Tsuchiya R, Tsuchida N, Fushimi M, Sekiya T, Nishimura S (1984) A novel combination of K-ras andmyc amplification accompanied by point mutational activation of K-ras in a human lung cancer. EMBO J 3: 2943–2946PubMedGoogle Scholar
  78. Toda T, Uno I, Ishikawa T, Powers S, Kataoka T, Broek D, Cameron S Broach J, Matsumoto K, Wigler M (1985) In yeast, Ras proteins are controlling elements of adenylate cyclase. Cell 40: 27–36PubMedCrossRefGoogle Scholar
  79. Tybulewicz VLJ, Falk G, Walker JE (1984)Rhodopseudomonas blastica atp operon: Nucleotide sequence and transcription. J Mol Biol 179: 185–214PubMedCrossRefGoogle Scholar
  80. van den Berg EA, Geerse RH, Memelink J, Bovenberg RAL, Magnee FA, van de Putte P (1985) Analysis of regulatory sequences upstream of theE. coli uvrB gene; involvement of the DnaA protein. Nucleic Acids Res 13: 1829–1840PubMedGoogle Scholar
  81. Varley JM, Boulnois GJ (1984) Analysis of a cloned colicin Ib gene: complete nucleotide sequence and implications for regulation of expression. Nucleic Acids Res 12: 6727–6739PubMedGoogle Scholar
  82. Vasautha N, Thompson LD, Rhodes C, Banner C, Nagle J, Filpula D (1984) Genes for alkaline protease and neutral protease fromBacillus amyloliquefaciens contain a large open reading frame between the regions coding for signal sequence and mature protein. J Bacteriol 159: 811–819Google Scholar
  83. Walker GC (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage inE. coli. Microbiol Rev 48: 60–93PubMedGoogle Scholar
  84. Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the α and β subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1: 945–951PubMedGoogle Scholar
  85. Ward JE, Lutkenhaus JF (1984) ThelacZ-ftsZ gene fusion is an analog of the cell division inhibitorsulA. J Bacteriol 157: 815–820PubMedGoogle Scholar
  86. Wertman KF, Mount DW (1985) Nucleotide sequence binding specificity of the LexA repressor ofE. coli K-12. J Bacteriol 163: 376–384PubMedGoogle Scholar
  87. Wierenga RK, Hol WGJ (1983) Predicted nucleotide binding properties of p21 protein and its cancer-associated variant. Nature 302: 842–844PubMedCrossRefGoogle Scholar
  88. Wilbur WJ, Lipman DJ (1983) Rapid similarity searches of nucleic acid and protein data bank. Proc Natl Acad Sci USA 80: 726–730PubMedCrossRefGoogle Scholar
  89. Yanofsky C, Platt T, Crawford IP, Nichols BP, Christie GE, Horowitz H, VanCleemput M, Wu AM (1981) The complete nucleotide sequence of the tryptophan operon ofE. coli. Nucleic Acids Res 24: 6647–6668Google Scholar
  90. Yi Q-M, Rockenbach S, Ward JE, Lutkenhaus J (1985) Structure and expression of the cell division genesftsQ,ftsA andftsZ. J Mol Biol 184: 399–412PubMedCrossRefGoogle Scholar
  91. Zarbl H, Sukumar S, Arthur AV, Martin-Zanca D, Barbacus M (1985) Direct mutagenesis of Ha-ras-1 oncogenes by N-nitroso-N-methylurea during initiation of mammary carcinogenesis in rats. Nature 315: 382–385PubMedCrossRefGoogle Scholar
  92. Zurawski G, Bottomley W, Whitfield PR (1982) Structures of the genes for the β and ε subunits of spinach chloroplast ATPase indicates a dicistronic MRNA and an overlapping transplation stop/start signal. Proc Natl Acad Sci USA 79: 6260–6264PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • Deborah R. Gill
    • 1
  • Graham F. Hatfull
    • 2
  • George P. C. Salmond
    • 1
  1. 1.Department of Biological SciencesUniversity of WarwickCoventryUK
  2. 2.MRC Laboratory of Molecular BiologyCambridgeUK
  3. 3.Department of Molecular Biophysics and BiochemistryYale University School of MedicineNew HavenUSA

Personalised recommendations