Abstract
A mutation in a newly discovered Escherichia coli cell division gene, ftsK, causes a temperature-sensitive late-stage block in division but does not affect chromosome replication or segregation. This defect is specifically suppressed by deletion of dacA, coding for the peptidoglycan DD-carboxypeptidase, PBP 5. FtsK is a large polypeptide (147 kDa) consisting of an N-terminal domain with several predicted membrane-spanning regions, a proline-glutamine-rich domain, and a C-terminal domain with a nucleotide-binding consensus sequence. FtsK has extensive sequence identity with a family of proteins from a wide variety of prokaryotes and plasmids. The plasmid proteins are required for intercellular DNA transfer, and one of the bacterial proteins (the SpoIIIE protein of Bacillus subtilis) has also been implicated in intracellular chromosomal DNA transfer.
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- Adler H. I., Fisher W. D., Cohen A., Hardigree A. A. MINIATURE escherichia coli CELLS DEFICIENT IN DNA. Proc Natl Acad Sci U S A. 1967 Feb;57(2):321–326. doi: 10.1073/pnas.57.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Altschul S. F., Boguski M. S., Gish W., Wootton J. C. Issues in searching molecular sequence databases. Nat Genet. 1994 Feb;6(2):119–129. doi: 10.1038/ng0294-119. [DOI] [PubMed] [Google Scholar]
- Bartecchi C. E., MacKenzie T. D., Schrier R. W. The global tobacco epidemic. Sci Am. 1995 May;272(5):44–51. doi: 10.1038/scientificamerican0595-44. [DOI] [PubMed] [Google Scholar]
- Beck B. D., Park J. T. Activity of three murein hydrolases during the cell division cycle of Escherichia coli K-12 as measured in toluene-treated cells. J Bacteriol. 1976 Jun;126(3):1250–1260. doi: 10.1128/jb.126.3.1250-1260.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Begg K. J., Donachie W. D. Cell shape and division in Escherichia coli: experiments with shape and division mutants. J Bacteriol. 1985 Aug;163(2):615–622. doi: 10.1128/jb.163.2.615-622.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Begg K. J., Donachie W. D. Experiments on chromosome separation and positioning in Escherichia coli. New Biol. 1991 May;3(5):475–486. [PubMed] [Google Scholar]
- Begg K. J., Hatfull G. F., Donachie W. D. Identification of new genes in a cell envelope-cell division gene cluster of Escherichia coli: cell division gene ftsQ. J Bacteriol. 1980 Oct;144(1):435–437. doi: 10.1128/jb.144.1.435-437.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Begg K. J., Spratt B. G., Donachie W. D. Interaction between membrane proteins PBP3 and rodA is required for normal cell shape and division in Escherichia coli. J Bacteriol. 1986 Sep;167(3):1004–1008. doi: 10.1128/jb.167.3.1004-1008.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Begg K. J., Takasuga A., Edwards D. H., Dewar S. J., Spratt B. G., Adachi H., Ohta T., Matsuzawa H., Donachie W. D. The balance between different peptidoglycan precursors determines whether Escherichia coli cells will elongate or divide. J Bacteriol. 1990 Dec;172(12):6697–6703. doi: 10.1128/jb.172.12.6697-6703.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Borodovsky M., Koonin E. V., Rudd K. E. New genes in old sequence: a strategy for finding genes in the bacterial genome. Trends Biochem Sci. 1994 Aug;19(8):309–313. doi: 10.1016/0968-0004(94)90067-1. [DOI] [PubMed] [Google Scholar]
- Bramhill D., Thompson C. M. GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5813–5817. doi: 10.1073/pnas.91.13.5813. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Broome-Smith J. K. Construction of a mutant of Escherichia coli that has deletions of both the penicillin-binding protein 5 and 6 genes. J Gen Microbiol. 1985 Aug;131(8):2115–2118. doi: 10.1099/00221287-131-8-2115. [DOI] [PubMed] [Google Scholar]
- Bukau B., Walker G. C. Cellular defects caused by deletion of the Escherichia coli dnaK gene indicate roles for heat shock protein in normal metabolism. J Bacteriol. 1989 May;171(5):2337–2346. doi: 10.1128/jb.171.5.2337-2346.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Claros M. G., von Heijne G. TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci. 1994 Dec;10(6):685–686. doi: 10.1093/bioinformatics/10.6.685. [DOI] [PubMed] [Google Scholar]
- Daniel R. A., Drake S., Buchanan C. E., Scholle R., Errington J. The Bacillus subtilis spoVD gene encodes a mother-cell-specific penicillin-binding protein required for spore morphogenesis. J Mol Biol. 1994 Jan 7;235(1):209–220. doi: 10.1016/s0022-2836(05)80027-0. [DOI] [PubMed] [Google Scholar]
- Donachie W. D., Begg K. J. Cell length, nucleoid separation, and cell division of rod-shaped and spherical cells of Escherichia coli. J Bacteriol. 1989 Sep;171(9):4633–4639. doi: 10.1128/jb.171.9.4633-4639.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Donachie W. D., Begg K. J. Chromosome partition in Escherichia coli requires postreplication protein synthesis. J Bacteriol. 1989 Oct;171(10):5405–5409. doi: 10.1128/jb.171.10.5405-5409.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Donachie W. D. The cell cycle of Escherichia coli. Annu Rev Microbiol. 1993;47:199–230. doi: 10.1146/annurev.mi.47.100193.001215. [DOI] [PubMed] [Google Scholar]
- Flannagan S. E., Zitzow L. A., Su Y. A., Clewell D. B. Nucleotide sequence of the 18-kb conjugative transposon Tn916 from Enterococcus faecalis. Plasmid. 1994 Nov;32(3):350–354. doi: 10.1006/plas.1994.1077. [DOI] [PubMed] [Google Scholar]
- Hagège J., Pernodet J. L., Sezonov G., Gerbaud C., Friedmann A., Guérineau M. Transfer functions of the conjugative integrating element pSAM2 from Streptomyces ambofaciens: characterization of a kil-kor system associated with transfer. J Bacteriol. 1993 Sep;175(17):5529–5538. doi: 10.1128/jb.175.17.5529-5538.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Huisman O., D'Ari R. An inducible DNA replication-cell division coupling mechanism in E. coli. Nature. 1981 Apr 30;290(5809):797–799. doi: 10.1038/290797a0. [DOI] [PubMed] [Google Scholar]
- Kendall K. J., Cohen S. N. Complete nucleotide sequence of the Streptomyces lividans plasmid pIJ101 and correlation of the sequence with genetic properties. J Bacteriol. 1988 Oct;170(10):4634–4651. doi: 10.1128/jb.170.10.4634-4651.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Khattar M. M., Begg K. J., Donachie W. D. Identification of FtsW and characterization of a new ftsW division mutant of Escherichia coli. J Bacteriol. 1994 Dec;176(23):7140–7147. doi: 10.1128/jb.176.23.7140-7147.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
- Lewis L. K., Jenkins M. E., Mount D. W. Isolation of DNA damage-inducible promoters in Escherichia coli: regulation of polB (dinA), dinG, and dinH by LexA repressor. J Bacteriol. 1992 May;174(10):3377–3385. doi: 10.1128/jb.174.10.3377-3385.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lin R., D'Ari R., Newman E. B. Lambda placMu insertions in genes of the leucine regulon: extension of the regulon to genes not regulated by leucine. J Bacteriol. 1992 Mar;174(6):1948–1955. doi: 10.1128/jb.174.6.1948-1955.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lutkenhaus J. F., Wolf-Watz H., Donachie W. D. Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ). J Bacteriol. 1980 May;142(2):615–620. doi: 10.1128/jb.142.2.615-620.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Markiewicz Z., Broome-Smith J. K., Schwarz U., Spratt B. G. Spherical E. coli due to elevated levels of D-alanine carboxypeptidase. Nature. 1982 Jun 24;297(5868):702–704. doi: 10.1038/297702a0. [DOI] [PubMed] [Google Scholar]
- Masters M., Colloms M. D., Oliver I. R., He L., Macnaughton E. J., Charters Y. The pcnB gene of Escherichia coli, which is required for ColE1 copy number maintenance, is dispensable. J Bacteriol. 1993 Jul;175(14):4405–4413. doi: 10.1128/jb.175.14.4405-4413.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matsuhashi M., Tamaki S., Curtis S. J., Strominger J. L. Mutational evidence for identity of penicillin-binding protein 5 in Escherichia coli with the major D-alanine carboxypeptidase IA activity. J Bacteriol. 1979 Jan;137(1):644–647. doi: 10.1128/jb.137.1.644-647.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Mukherjee A., Dai K., Lutkenhaus J. Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):1053–1057. doi: 10.1073/pnas.90.3.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mukherjee A., Lutkenhaus J. Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol. 1994 May;176(9):2754–2758. doi: 10.1128/jb.176.9.2754-2758.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Okita T. W., Cheesbrough V., Reeves C. D. Evolution and heterogeneity of the alpha-/beta-type and gamma-type gliadin DNA sequences. J Biol Chem. 1985 Jul 5;260(13):8203–8213. [PubMed] [Google Scholar]
- 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]
- Pisabarro A. G., Prats R., Váquez D., Rodríguez-Tébar A. Activity of penicillin-binding protein 3 from Escherichia coli. J Bacteriol. 1986 Oct;168(1):199–206. doi: 10.1128/jb.168.1.199-206.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- RayChaudhuri D., Park J. T. Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature. 1992 Sep 17;359(6392):251–254. doi: 10.1038/359251a0. [DOI] [PubMed] [Google Scholar]
- Robinson A. C., Begg K. J., Sweeney J., Condie A., Donachie W. D. Mapping and characterization of mutants of the Escherichia coli cell division gene, ftsA. Mol Microbiol. 1988 Sep;2(5):581–588. doi: 10.1111/j.1365-2958.1988.tb00066.x. [DOI] [PubMed] [Google Scholar]
- Russel M., Model P. Sequence of thioredoxin reductase from Escherichia coli. Relationship to other flavoprotein disulfide oxidoreductases. J Biol Chem. 1988 Jun 25;263(18):9015–9019. [PubMed] [Google Scholar]
- Singer M., Baker T. A., Schnitzler G., Deischel S. M., Goel M., Dove W., Jaacks K. J., Grossman A. D., Erickson J. W., Gross C. A. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev. 1989 Mar;53(1):1–24. doi: 10.1128/mr.53.1.1-24.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spratt B. G. Deletion of the penicillin-binding protein 5 gene of Escherichia coli. J Bacteriol. 1980 Dec;144(3):1190–1192. doi: 10.1128/jb.144.3.1190-1192.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Su Y. A., Clewell D. B. Characterization of the left 4 kb of conjugative transposon Tn916: determinants involved in excision. Plasmid. 1993 Nov;30(3):234–250. doi: 10.1006/plas.1993.1055. [DOI] [PubMed] [Google Scholar]
- Tatham A. S., Drake A. F., Shewry P. R. A conformational study of a glutamine- and proline-rich cereal seed protein, C hordein. Biochem J. 1985 Mar 1;226(2):557–562. doi: 10.1042/bj2260557. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tatham A. S., Drake A. F., Shewry P. R. Conformational studies of a synthetic peptide corresponding to the repeat motif of C hordein. Biochem J. 1989 Apr 15;259(2):471–476. doi: 10.1042/bj2590471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tomura T., Kishino H., Doi K., Hara T., Kuhara S., Ogata S. Sporulation-inhibitory gene in pock-forming plasmid pSA1.1 of Streptomyces azureus. Biosci Biotechnol Biochem. 1993 Mar;57(3):438–443. doi: 10.1271/bbb.57.438. [DOI] [PubMed] [Google Scholar]
- Tuan L. R., D'Ari R., Newman E. B. The leucine regulon of Escherichia coli K-12: a mutation in rblA alters expression of L-leucine-dependent metabolic operons. J Bacteriol. 1990 Aug;172(8):4529–4535. doi: 10.1128/jb.172.8.4529-4535.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walker J. E., Saraste M., Runswick M. J., Gay N. J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. doi: 10.1002/j.1460-2075.1982.tb01276.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang Q., Calvo J. M. Lrp, a global regulatory protein of Escherichia coli, binds co-operatively to multiple sites and activates transcription of ilvIH. J Mol Biol. 1993 Jan 20;229(2):306–318. doi: 10.1006/jmbi.1993.1036. [DOI] [PubMed] [Google Scholar]
- Wang Q., Calvo J. M. Lrp, a major regulatory protein in Escherichia coli, bends DNA and can organize the assembly of a higher-order nucleoprotein structure. EMBO J. 1993 Jun;12(6):2495–2501. doi: 10.1002/j.1460-2075.1993.tb05904.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang Q., Wu J., Friedberg D., Plakto J., Calvo J. M. Regulation of the Escherichia coli lrp gene. J Bacteriol. 1994 Apr;176(7):1831–1839. doi: 10.1128/jb.176.7.1831-1839.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Willins D. A., Ryan C. W., Platko J. V., Calvo J. M. Characterization of Lrp, and Escherichia coli regulatory protein that mediates a global response to leucine. J Biol Chem. 1991 Jun 15;266(17):10768–10774. [PubMed] [Google Scholar]
- Wolf-Watz H., Normark S. Evidence for a role of N-acetylmuramyl-L-alanine amidase in septum separation in Escherichia coli. J Bacteriol. 1976 Nov;128(2):580–586. doi: 10.1128/jb.128.2.580-586.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- de Boer P., Crossley R., Rothfield L. The essential bacterial cell-division protein FtsZ is a GTPase. Nature. 1992 Sep 17;359(6392):254–256. doi: 10.1038/359254a0. [DOI] [PubMed] [Google Scholar]