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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
. 1979 Sep;76(9):4669–4673. doi: 10.1073/pnas.76.9.4669

Requirement for membrane potential in injection of phage T4 DNA.

B Labedan, E B Goldberg
PMCID: PMC411642  PMID: 41245

Abstract

The first stages of infection by phage T4 may be divided into energy-dependent and energy-independent processes. Irreversible adsorption, unplugging, and initial exposure of the DNA terminus may occur at 4 degrees C, or at 37 degrees C in bacteria whose energy-yielding metabolism has been poisoned. DNA injection into the cytoplasm needs higher temperatures and energy from the host cell. The nature of this energy requirements was deduced from the use of metabolic inhibitors. Our results show that T4 DNA injection specifically requires the presence of a protonmotive force across the cytoplasmic membrane of the host. Moreover, the chemical gradient (delta pH) does not appear to be essential, but the membrane potential (delta psi) is required.

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Selected References

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

  1. CHRISTENSEN J. R., TOLMACH L. J. On the early stages of infection of Escherichia coli B by bacteriophage T1. Arch Biochem Biophys. 1955 Jul;57(1):195–207. doi: 10.1016/0003-9861(55)90192-2. [DOI] [PubMed] [Google Scholar]
  2. Crawford J. T., Goldberg E. B. The effect of baseplate mutations on the requirement for tail-fiber binding for irreversible adsorption of bacteriophage T4. J Mol Biol. 1977 Apr 15;111(3):305–313. doi: 10.1016/s0022-2836(77)80053-3. [DOI] [PubMed] [Google Scholar]
  3. Dharmalingam K., Goldberg E. B. Mechanism localisation and control of restriction cleavage of phage T4 and lambda chromosomes in vivo. Nature. 1976 Apr 1;260(5550):406–410. doi: 10.1038/260406a0. [DOI] [PubMed] [Google Scholar]
  4. Grinius L. L. Khemiosmoticheskii mekhanizm transporta biologicheskikh makromolekul cherez membrany bakterii. Biokhimiia. 1976 Sep;41(9):1539–1547. [PubMed] [Google Scholar]
  5. Grinius L., Berzinskiene J. Studies on DNA transport during bacterial conjugation. Role of protonmotive force-generating H+-ATPase and respiratory chain. FEBS Lett. 1976 Dec 15;72(1):151–154. doi: 10.1016/0014-5793(76)80833-2. [DOI] [PubMed] [Google Scholar]
  6. HERSHEY A. D., CHASE M. Independent functions of viral protein and nucleic acid in growth of bacteriophage. J Gen Physiol. 1952 May;36(1):39–56. doi: 10.1085/jgp.36.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hancock R. W., Braun V. Nature of the energy requirement for the irreversible adsorption of bacteriophages T1 and phi80 to Escherichia coli. J Bacteriol. 1976 Feb;125(2):409–415. doi: 10.1128/jb.125.2.409-415.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Harold F. M. Conservation and transformation of energy by bacterial membranes. Bacteriol Rev. 1972 Jun;36(2):172–230. doi: 10.1128/br.36.2.172-230.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hendrix R. W. Symmetry mismatch and DNA packaging in large bacteriophages. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4779–4783. doi: 10.1073/pnas.75.10.4779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hirokawa H. Transfecting deoxyribonucleic acid of Bacillus bacteriophage phi 29 that is protease sensitive. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1555–1559. doi: 10.1073/pnas.69.6.1555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Israel V. E proteins of bacteriophage P22. I. Identification and ejection from wild-type and defective particles. J Virol. 1977 Jul;23(1):91–97. doi: 10.1128/jvi.23.1.91-97.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jazwinski S. M., Lindberg A. A., Kornberg A. The gene H spike protein of bacteriophages phiX174 and S13. I. Functions in phage-receptor recognition and in transfection. Virology. 1975 Jul;66(1):283–293. doi: 10.1016/0042-6822(75)90198-1. [DOI] [PubMed] [Google Scholar]
  13. Kaback H. R., Reeves J. P., Short S. A., Lombardi F. J. Mechanisms of active transport in isolated bacterial membrane vesicles. 18. The mechanism of action of carbonylcyanide m-chlorophenylhydrazone. Arch Biochem Biophys. 1974 Jan;160(1):215–222. doi: 10.1016/s0003-9861(74)80028-7. [DOI] [PubMed] [Google Scholar]
  14. Kalasauskaite E., Grinius L. The role of energy-yielding ATPase and respiratory chain at early stages of bacteriophage T4 infection. FEBS Lett. 1979 Mar 15;99(2):287–291. doi: 10.1016/0014-5793(79)80974-6. [DOI] [PubMed] [Google Scholar]
  15. Klein W. L., Boyer P. D. Energization of active transport by Escherichia coli. J Biol Chem. 1972 Nov 25;247(22):7257–7265. [PubMed] [Google Scholar]
  16. Labedan B. A very early step in the T5 DNA injection process. Virology. 1976 Dec;75(2):368–375. doi: 10.1016/0042-6822(76)90035-0. [DOI] [PubMed] [Google Scholar]
  17. Leipold B., Hofschneider P. H. Isolation of an infectious RNA-A-protein complex from the bacteriophage M12. FEBS Lett. 1975 Jul 15;55(1):50–52. doi: 10.1016/0014-5793(75)80954-9. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Mitchell P. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev Camb Philos Soc. 1966 Aug;41(3):445–502. doi: 10.1111/j.1469-185x.1966.tb01501.x. [DOI] [PubMed] [Google Scholar]
  20. Oliver D. B., Goldberg E. B. Protection of parental T4 DNA from a restriction exonuclease by the product of gene 2. J Mol Biol. 1977 Nov;116(4):877–881. doi: 10.1016/0022-2836(77)90276-5. [DOI] [PubMed] [Google Scholar]
  21. Ortin J., Viñuela E., Salas M., Vasquez C. DNA-protein complex in circular DNA from phage phi-29. Nat New Biol. 1971 Dec 29;234(52):275–277. doi: 10.1038/newbio234275a0. [DOI] [PubMed] [Google Scholar]
  22. Plate C. A. Requirement for membrane potential in active transport of glutamine by Escherichia coli. J Bacteriol. 1979 Jan;137(1):221–225. doi: 10.1128/jb.137.1.221-225.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Plate C. A., Suit J. L., Jetten A. M., Luria S. E. Effects of colicin K on a mutant of Escherichia coli deficient in Ca 2+, Mg 2+-activated adenosine triphosphatase. J Biol Chem. 1974 Oct 10;249(19):6138–6143. [PubMed] [Google Scholar]
  24. Pudek M. R., Bragg P. D. Reaction of cyanide with cytochrome d in respiratory particles from exponential phase Escherichia coli. FEBS Lett. 1975 Feb 1;50(2):111–113. doi: 10.1016/0014-5793(75)80468-6. [DOI] [PubMed] [Google Scholar]
  25. Ramos S., Kaback H. R. The electrochemical proton gradient in Escherichia coli membrane vesicles. Biochemistry. 1977 Mar 8;16(5):848–854. doi: 10.1021/bi00624a006. [DOI] [PubMed] [Google Scholar]
  26. Renthal R., Lanyi J. K. Light-induced membrane potential and pH gradient in Halobacterium halobium envelope vesicles. Biochemistry. 1976 May 18;15(10):2136–2143. doi: 10.1021/bi00655a017. [DOI] [PubMed] [Google Scholar]
  27. Rinehart C. A., Hubbard J. S. Energy coupling in the active transport of proline and glutamate by the photosynthetic halophile Ectothiorhodospira halophila. J Bacteriol. 1976 Sep;127(3):1255–1264. doi: 10.1128/jb.127.3.1255-1264.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Silverstein J. L., Goldberg E. B. T4 DNA injection. II. Protection of entering DNA from host exonuclease V. Virology. 1976 Jul 1;72(1):212–223. doi: 10.1016/0042-6822(76)90324-x. [DOI] [PubMed] [Google Scholar]
  29. Simon L. D., Anderson T. F. The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. I. Attachment and penetration. Virology. 1967 Jun;32(2):279–297. doi: 10.1016/0042-6822(67)90277-2. [DOI] [PubMed] [Google Scholar]
  30. Strauss N. Early energy-dependent step in the entry of transforming deoxyribonucleic acid. J Bacteriol. 1970 Jan;101(1):35–37. doi: 10.1128/jb.101.1.35-37.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Toro M., Gómez-Lojero C., Montal M., Estrada-O S. Charge transfer mediated by nigericin in black lipid membranes. J Bioenerg. 1976 Feb;8(1):19–26. doi: 10.1007/BF01559387. [DOI] [PubMed] [Google Scholar]
  32. Wais A. C., Goldberg E. B. Growth and transformation of phage T4 in Escherichia coli B-4, Salmonella, Aerobacter, Proteus, and Serratia. Virology. 1969 Oct;39(2):153–161. doi: 10.1016/0042-6822(69)90035-x. [DOI] [PubMed] [Google Scholar]
  33. Weiss M. J., Luria S. E. Reduction of membrane potential, an immediate effect of colicin K. Proc Natl Acad Sci U S A. 1978 May;75(5):2483–2487. doi: 10.1073/pnas.75.5.2483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wilson J. H., Luftig R. B., Wood W. B. Interaction of bacteriophage T4 tail fiber components with a lipopolysaccharide fraction from Escherichia coli. J Mol Biol. 1970 Jul 28;51(2):423–434. doi: 10.1016/0022-2836(70)90152-x. [DOI] [PubMed] [Google Scholar]
  35. Zilberstein D., Schuldiner S., Padan E. Proton electrochemical gradient in Escherichia coli cells and its relation to active transport of lactose. Biochemistry. 1979 Feb 20;18(4):669–673. doi: 10.1021/bi00571a018. [DOI] [PubMed] [Google Scholar]
  36. Zárybnický V. Mechanism of T-even DNA ejection. J Theor Biol. 1969 Jan;22(1):33–42. doi: 10.1016/0022-5193(69)90078-2. [DOI] [PubMed] [Google Scholar]

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