Abstract
The nature of resistance to phage T2 in Escherichia coli K-12 was investigated by analyzing a known phage T2-resistant mutant and by isolating new T2-resistant mutants. It was found that mutational alterations at two loci, ompF (encoding the outer membrane protein OmpF) and ttr (T-two resistance), are needed to give full resistance to phage T2. A ttr::Tn10 mutation was isolated and was mapped between aroC and dsdA, where the fadL gene (required for long-chain fatty acid transport) is located. The receptor affected by ttr was the major receptor used by phage T2 and was located in the outer membrane. Phage T2 was thus able to use two outer membrane proteins as receptors. All strains having a ttr::Tn10 allele and most of the independently isolated phage T2-resistant mutants were unable to grow on oleate as the sole carbon and energy source, i.e., they had the phenotype of fadL mutants. The gene fadL is known to encode an inner membrane protein. The most likely explanation is that fadL and ttr are in an operon and that ttr encodes an outer membrane protein which functions in translocating long-chain fatty acids across the outer membrane and also as a receptor for phage T2.
Full text
PDF






Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- Bachmann B. J., Low K. B. Linkage map of Escherichia coli K-12, edition 6. Microbiol Rev. 1980 Mar;44(1):1–56. doi: 10.1128/mr.44.1.1-56.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beher M. G., Pugsley A. P. Coliphage which requires either the LamB protein or the OmpC protein for adsorption to Escherichia coli K-12. J Virol. 1981 Apr;38(1):372–375. doi: 10.1128/jvi.38.1.372-375.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Black P. N., Kianian S. F., DiRusso C. C., Nunn W. D. Long-chain fatty acid transport in Escherichia coli. Cloning, mapping, and expression of the fadL gene. J Biol Chem. 1985 Feb 10;260(3):1780–1789. [PubMed] [Google Scholar]
- Cozzarelli N. R., Freedberg W. B., Lin E. C. Genetic control of L-alpha-glycerophosphate system in Escherichia coli. J Mol Biol. 1968 Feb 14;31(3):371–387. doi: 10.1016/0022-2836(68)90415-4. [DOI] [PubMed] [Google Scholar]
- Datta D. B., Arden B., Henning U. Major proteins of the Escherichia coli outer cell envelope membrane as bacteriophage receptors. J Bacteriol. 1977 Sep;131(3):821–829. doi: 10.1128/jb.131.3.821-829.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Foster T. J., Lundblad V., Hanley-Way S., Halling S. M., Kleckner N. Three Tn10-associated excision events: relationship to transposition and role of direct and inverted repeats. Cell. 1981 Jan;23(1):215–227. doi: 10.1016/0092-8674(81)90286-5. [DOI] [PubMed] [Google Scholar]
- Ginsburgh C. L., Black P. N., Nunn W. D. Transport of long chain fatty acids in Escherichia coli. Identification of a membrane protein associated with the fadL gene. J Biol Chem. 1984 Jul 10;259(13):8437–8443. [PubMed] [Google Scholar]
- Hancock R. E., Reeves P. Bacteriophage resistance in Escherichia coli K-12: general pattern of resistance. J Bacteriol. 1975 Mar;121(3):983–993. doi: 10.1128/jb.121.3.983-993.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hantke K. Major outer membrane proteins of E. coli K12 serve as receptors for the phages T2 (protein Ia) and 434 (protein Ib). Mol Gen Genet. 1978 Aug 17;164(2):131–135. doi: 10.1007/BF00267377. [DOI] [PubMed] [Google Scholar]
- Ish-Horowicz D., Burke J. F. Rapid and efficient cosmid cloning. Nucleic Acids Res. 1981 Jul 10;9(13):2989–2998. doi: 10.1093/nar/9.13.2989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Lenski R. E. Two-step resistance by Escherichia coli B to bacteriophage T2. Genetics. 1984 May;107(1):1–7. doi: 10.1093/genetics/107.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Lugtenberg B., Van Alphen L. Molecular architecture and functioning of the outer membrane of Escherichia coli and other gram-negative bacteria. Biochim Biophys Acta. 1983 Mar 21;737(1):51–115. doi: 10.1016/0304-4157(83)90014-x. [DOI] [PubMed] [Google Scholar]
- Lundrigan M. D., Earhart C. F. Gene envY of Escherichia coli K-12 affects thermoregulation of major porin expression. J Bacteriol. 1984 Jan;157(1):262–268. doi: 10.1128/jb.157.1.262-268.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maloy S. R., Ginsburgh C. L., Simons R. W., Nunn W. D. Transport of long and medium chain fatty acids by Escherichia coli K12. J Biol Chem. 1981 Apr 25;256(8):3735–3742. [PubMed] [Google Scholar]
- Manning P. A., Beutin L., Achtman M. Outer membrane of Escherichia coli: properties of the F sex factor traT protein which is involved in surface exclusion. J Bacteriol. 1980 Apr;142(1):285–294. doi: 10.1128/jb.142.1.285-294.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Manoil C. A genetic approach to defining the sites of interaction of a membrane protein with different external agents. J Mol Biol. 1983 Sep 15;169(2):507–519. doi: 10.1016/s0022-2836(83)80063-1. [DOI] [PubMed] [Google Scholar]
- Moreno F., Wandersman C. OmpC and LamB proteins can serve as substitute receptors for host range mutants of coliphage TuIa. J Bacteriol. 1980 Dec;144(3):1182–1185. doi: 10.1128/jb.144.3.1182-1185.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morona R., Henning U. Host range mutants of bacteriophage Ox2 can use two different outer membrane proteins of Escherichia coli K-12 as receptors. J Bacteriol. 1984 Aug;159(2):579–582. doi: 10.1128/jb.159.2.579-582.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morona R., Klose M., Henning U. Escherichia coli K-12 outer membrane protein (OmpA) as a bacteriophage receptor: analysis of mutant genes expressing altered proteins. J Bacteriol. 1984 Aug;159(2):570–578. doi: 10.1128/jb.159.2.570-578.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morona R., Reeves P. Molecular cloning of the tolC locus of Escherichia coli K-12 with the use of transposon Tn10. Mol Gen Genet. 1981;184(3):430–433. doi: 10.1007/BF00352517. [DOI] [PubMed] [Google Scholar]
- Morona R., Reeves P. The tolC locus of Escherichia coli affects the expression of three major outer membrane proteins. J Bacteriol. 1982 Jun;150(3):1016–1023. doi: 10.1128/jb.150.3.1016-1023.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morona R., Tommassen J., Henning U. Demonstration of a bacteriophage receptor site on the Escherichia coli K12 outer-membrane protein OmpC by the use of a protease. Eur J Biochem. 1985 Jul 1;150(1):161–169. doi: 10.1111/j.1432-1033.1985.tb09002.x. [DOI] [PubMed] [Google Scholar]
- Nunn W. D., Simons R. W. Transport of long-chain fatty acids by Escherichia coli: mapping and characterization of mutants in the fadL gene. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3377–3381. doi: 10.1073/pnas.75.7.3377. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Puspurs A., Medon P., Corless C., Hackett J., Reeves P. A class of ompA mutants of Escherichia coli K12 affected in the interaction of ompA protein and the core region of lipopolysaccharide. Mol Gen Genet. 1983;189(1):162–165. doi: 10.1007/BF00326070. [DOI] [PubMed] [Google Scholar]
- REISSIG J. L., WOLLMAN E. L. TRANSDUCTION DES MARQUEURS GALACTOSE PAR LES BACT'ERIOPHAGES TEMP'ER'ES 82 ET 434 D'ESCHERICHIA COLI. Ann Inst Pasteur (Paris) 1963 Oct;105:774–779. [PubMed] [Google Scholar]
- Riede I., Degen M., Henning U. The receptor specificity of bacteriophages can be determined by a tail fiber modifying protein. EMBO J. 1985 Sep;4(9):2343–2346. doi: 10.1002/j.1460-2075.1985.tb03936.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmitges C. J., Henning U. The major proteins of the Escherichia coli outer cell-envelope membrane. Heterogeneity of protein I. Eur J Biochem. 1976 Mar 16;63(1):47–52. doi: 10.1111/j.1432-1033.1976.tb10205.x. [DOI] [PubMed] [Google Scholar]
- Silhavy T. J., Hartig-Beecken I., Boos W. Periplasmic protein related to the sn-glycerol-3-phosphate transport system of Escherichia coli. J Bacteriol. 1976 May;126(2):951–958. doi: 10.1128/jb.126.2.951-958.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wandersman C., Schwartz M. Protein Ia and the lamB protein can replace each other in the constitution of an active receptor for the same coliphage. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5636–5639. doi: 10.1073/pnas.75.11.5636. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson G. G., Young K. Y., Edlin G. J., Konigsberg W. High-frequency generalised transduction by bacteriophage T4. Nature. 1979 Jul 5;280(5717):80–82. doi: 10.1038/280080a0. [DOI] [PubMed] [Google Scholar]
- Yu F., Mizushima S. Roles of lipopolysaccharide and outer membrane protein OmpC of Escherichia coli K-12 in the receptor function for bacteriophage T4. J Bacteriol. 1982 Aug;151(2):718–722. doi: 10.1128/jb.151.2.718-722.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]