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. 1986 Jan;165(1):107–115. doi: 10.1128/jb.165.1.107-115.1986

fii, a bacterial locus required for filamentous phage infection and its relation to colicin-tolerant tolA and tolB.

T P Sun, R E Webster
PMCID: PMC214377  PMID: 3001021

Abstract

We describe mutations in a new bacterial locus, designated fii, which do not allow the filamentous bacteriophage f1 to infect bacteria harboring the F plasmid. Mutations at this locus do not affect the ability of F plasmid-containing bacteria to undergo conjugation or be infected by the F plasmid-specific RNA phage f2. The filamentous phage can still adsorb to the F sex pilus, but the DNA is unable to enter the bacteria. All fii mutants become tolerant to colicins E1, E2, and E3. Strains with amber mutations in fii also are unable to plaque P1, even though they can be infected with this phage. Mutations in fii also prevent infection of bacteria harboring the N plasmid by the filamentous bacteriophage IKe. The fii locus maps adjacent to tolA, mutants of which demonstrate tolerance to high levels of the E and K colicins. The three genes tolA, tolB, and fii are shown to reside on a 4.3-kilobase fragment of the Escherichia coli chromosome. Each gene has been cloned into a chimeric plasmid and shown to complement, in trans, mutations at the corresponding chromosomal locus. Studies in maxicells show that the product of fii appears to be a 24-kilodalton protein which copurifies with the cell envelope. The product of tolA has been identified tentatively as a 51-kilodalton protein. Data from cloning, Tn5 mutagenesis, and P1 transduction studies are consistent with the gene order sucA-fii-tolA-tolB-aroG near 17 min on the E. coli map.

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Selected References

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  1. Armstrong J., Perham R. N., Walker J. E. Domain structure of bacteriophage fd adsorption protein. FEBS Lett. 1981 Nov 30;135(1):167–172. doi: 10.1016/0014-5793(81)80969-6. [DOI] [PubMed] [Google Scholar]
  2. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 7. Microbiol Rev. 1983 Jun;47(2):180–230. doi: 10.1128/mr.47.2.180-230.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bernstein A., Rolfe B., Onodera K. Pleiotropic properties and genetic organization of the tolA,B locus of Escherichia coli K-12. J Bacteriol. 1972 Oct;112(1):74–83. doi: 10.1128/jb.112.1.74-83.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boeke J. D., Model P., Zinder N. D. Effects of bacteriophage f1 gene III protein on the host cell membrane. Mol Gen Genet. 1982;186(2):185–192. doi: 10.1007/BF00331849. [DOI] [PubMed] [Google Scholar]
  5. Burke J. M., Novotny C. P., Fives-Taylor P. Defective F pili and other characteristics of Flac and Hfr Escherichia coli mutants resistant to bacteriophage R17. J Bacteriol. 1979 Nov;140(2):525–531. doi: 10.1128/jb.140.2.525-531.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buxton R. S. Genetic analysis of Escherichia coli K12 mutants resistant to bacteriophage BF23 and the E-group colicins. Mol Gen Genet. 1971;113(2):154–156. doi: 10.1007/BF00333188. [DOI] [PubMed] [Google Scholar]
  7. Caro L. G., Schnös M. The attachment of the male-specific bacteriophage F1 to sensitive strains of Escherichia coli. Proc Natl Acad Sci U S A. 1966 Jul;56(1):126–132. doi: 10.1073/pnas.56.1.126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cheng S. C., Modrich P. Positive-selection cloning vehicle useful for overproduction of hybrid proteins. J Bacteriol. 1983 May;154(2):1005–1008. doi: 10.1128/jb.154.2.1005-1008.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cole S. T., Saint-Joanis B., Pugsley A. P. Molecular characterisation of the colicin E2 operon and identification of its products. Mol Gen Genet. 1985;198(3):465–472. doi: 10.1007/BF00332940. [DOI] [PubMed] [Google Scholar]
  10. Curtiss R., 3rd Bacterial conjugation. Annu Rev Microbiol. 1969;23:69–136. doi: 10.1146/annurev.mi.23.100169.000441. [DOI] [PubMed] [Google Scholar]
  11. Di Masi D. R., White J. C., Schnaitman C. A., Bradbeer C. Transport of vitamin B12 in Escherichia coli: common receptor sites for vitamin B12 and the E colicins on the outer membrane of the cell envelope. J Bacteriol. 1973 Aug;115(2):506–513. doi: 10.1128/jb.115.2.506-513.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. GAREN A., GAREN S. Genetic evidence on the nature of the repressor for alkaline phosphatase in E. coli. J Mol Biol. 1963 May;6:433–438. doi: 10.1016/s0022-2836(63)80054-6. [DOI] [PubMed] [Google Scholar]
  13. Goldsmith M. E., Konigsberg W. H. Adsorption protein of the bacteriophage fd: isolation, molecular properties, and location in the virus. Biochemistry. 1977 Jun 14;16(12):2686–2694. doi: 10.1021/bi00631a016. [DOI] [PubMed] [Google Scholar]
  14. Grant R. A., Lin T. C., Konigsberg W., Webster R. E. Structure of the filamentous bacteriophage fl. Location of the A, C, and D minor coat proteins. J Biol Chem. 1981 Jan 10;256(1):539–546. [PubMed] [Google Scholar]
  15. Gray C. W., Brown R. S., Marvin D. A. Adsorption complex of filamentous fd virus. J Mol Biol. 1981 Mar 15;146(4):621–627. doi: 10.1016/0022-2836(81)90050-4. [DOI] [PubMed] [Google Scholar]
  16. Jacobson A. Role of F pili in the penetration of bacteriophage fl. J Virol. 1972 Oct;10(4):835–843. doi: 10.1128/jvi.10.4.835-843.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kadner R. J., Liggins G. L. Transport of vitamin B12 in Escherichia coli: genetic studies. J Bacteriol. 1973 Aug;115(2):514–521. doi: 10.1128/jb.115.2.514-521.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kleckner N., Chan R. K., Tye B. K., Botstein D. Mutagenesis by insertion of a drug-resistance element carrying an inverted repetition. J Mol Biol. 1975 Oct 5;97(4):561–575. doi: 10.1016/s0022-2836(75)80059-3. [DOI] [PubMed] [Google Scholar]
  19. Low B. Rapid mapping of conditional and auxotrophic mutations in Escherichia coli K-12. J Bacteriol. 1973 Feb;113(2):798–812. doi: 10.1128/jb.113.2.798-812.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Marco R., Jazwinski S. M., Kornberg A. Binding, eclipse, and penetration of the filamentous bacteriophage M13 in intact and disrupted cells. Virology. 1974 Nov;62(1):209–223. doi: 10.1016/0042-6822(74)90316-x. [DOI] [PubMed] [Google Scholar]
  21. Marvin D. A., Hohn B. Filamentous bacterial viruses. Bacteriol Rev. 1969 Jun;33(2):172–209. doi: 10.1128/br.33.2.172-209.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Masaki H., Ohta T. A plasmid region encoding the active fragment and the inhibitor protein of colicin E3--CA38. FEBS Lett. 1982 Nov 22;149(1):129–132. doi: 10.1016/0014-5793(82)81087-9. [DOI] [PubMed] [Google Scholar]
  23. Mock M., Miyada C. G., Gunsalus R. P. Nucleotide sequence for the catalytic domain of colicin E3 and its immunity protein. Evidence for a third gene overlapping colicin. Nucleic Acids Res. 1983 Jun 11;11(11):3547–3557. doi: 10.1093/nar/11.11.3547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nagel de Zwaig R., Luria S. E. Genetics and physiology of colicin-tolerant mutants of Escherichia coli. J Bacteriol. 1967 Oct;94(4):1112–1123. doi: 10.1128/jb.94.4.1112-1123.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nelson F. K., Friedman S. M., Smith G. P. Filamentous phage DNA cloning vectors: a noninfective mutant with a nonpolar deletion in gene III. Virology. 1981 Jan 30;108(2):338–350. doi: 10.1016/0042-6822(81)90442-6. [DOI] [PubMed] [Google Scholar]
  26. Norrander J., Kempe T., Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. doi: 10.1016/0378-1119(83)90040-9. [DOI] [PubMed] [Google Scholar]
  27. Peeters B. P., Peters R. M., Schoenmakers J. G., Konings R. N. Nucleotide sequence and genetic organization of the genome of the N-specific filamentous bacteriophage IKe. Comparison with the genome of the F-specific filamentous phages M13, fd and f1. J Mol Biol. 1985 Jan 5;181(1):27–39. doi: 10.1016/0022-2836(85)90322-5. [DOI] [PubMed] [Google Scholar]
  28. Pratt D., Tzagoloff H., Erdahl W. S. Conditional lethal mutants of the small filamentous coliphage M13. I. Isolation, complementation, cell killing, time of cistron action. Virology. 1966 Nov;30(3):397–410. doi: 10.1016/0042-6822(66)90118-8. [DOI] [PubMed] [Google Scholar]
  29. Rossomando E. F. Studies on the structural polarity of bacteriophage f1. Virology. 1970 Nov;42(3):681–687. doi: 10.1016/0042-6822(70)90313-2. [DOI] [PubMed] [Google Scholar]
  30. Russel M., Model P. A bacterial gene, fip, required for filamentous bacteriophage fl assembly. J Bacteriol. 1983 Jun;154(3):1064–1076. doi: 10.1128/jb.154.3.1064-1076.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Russel M., Model P. A mutation downstream from the signal peptidase cleavage site affects cleavage but not membrane insertion of phage coat protein. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1717–1721. doi: 10.1073/pnas.78.3.1717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Russel M., Model P. Characterization of the cloned fip gene and its product. J Bacteriol. 1984 Feb;157(2):526–532. doi: 10.1128/jb.157.2.526-532.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sancar A., Hack A. M., Rupp W. D. Simple method for identification of plasmid-coded proteins. J Bacteriol. 1979 Jan;137(1):692–693. doi: 10.1128/jb.137.1.692-693.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Smilowitz H. Bacteriophage f1 infection and colicin tolerance. J Virol. 1974 Jan;13(1):100–106. doi: 10.1128/jvi.13.1.100-106.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Smilowitz H. Bacteriophage f1 infection: fate of the parental major coat protein. J Virol. 1974 Jan;13(1):94–99. doi: 10.1128/jvi.13.1.94-99.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Smith H. O., Birnstiel M. L. A simple method for DNA restriction site mapping. Nucleic Acids Res. 1976 Sep;3(9):2387–2398. doi: 10.1093/nar/3.9.2387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. TZAGOLOFF H., PRATT D. THE INITIAL STEPS IN INFECTION WITH COLIPHAGE M13. Virology. 1964 Nov;24:372–380. doi: 10.1016/0042-6822(64)90174-6. [DOI] [PubMed] [Google Scholar]
  38. Trenkner E., Bonhoeffer F., Gierer A. The fate of the protein component of bacteriophage fd during infection. Biochem Biophys Res Commun. 1967 Sep 27;28(6):932–939. doi: 10.1016/0006-291x(67)90069-1. [DOI] [PubMed] [Google Scholar]
  39. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  40. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  41. Viñuela E., Algranati I. D., Ochoa S. Synthesis of virus-specific proteins in Escherichia coli infected with the RNA bacteriophage MS2. Eur J Biochem. 1967 Mar;1(1):3–11. doi: 10.1007/978-3-662-25813-2_2. [DOI] [PubMed] [Google Scholar]
  42. Willetts N., Skurray R. The conjugation system of F-like plasmids. Annu Rev Genet. 1980;14:41–76. doi: 10.1146/annurev.ge.14.120180.000353. [DOI] [PubMed] [Google Scholar]
  43. Woolford J. L., Jr, Steinman H. M., Webster R. E. Adsorption protein of bacteriophage fl: solubilization in deoxycholate and localization in the fl virion. Biochemistry. 1977 Jun 14;16(12):2694–2700. doi: 10.1021/bi00631a017. [DOI] [PubMed] [Google Scholar]
  44. Yamada M., Ebina Y., Miyata T., Nakazawa T., Nakazawa A. Nucleotide sequence of the structural gene for colicin E1 and predicted structure of the protein. Proc Natl Acad Sci U S A. 1982 May;79(9):2827–2831. doi: 10.1073/pnas.79.9.2827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zinder N. D. Resistance to colicins E3 and K induced by infection with bacteriophage f1. Proc Natl Acad Sci U S A. 1973 Nov;70(11):3160–3164. doi: 10.1073/pnas.70.11.3160. [DOI] [PMC free article] [PubMed] [Google Scholar]

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