Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1977 Jun;130(3):1214–1223. doi: 10.1128/jb.130.3.1214-1223.1977

Genetics of Sensitivity of Salmonella Species to Colicin M and Bacteriophages T5, T1, and ES18

Amy C Graham a,1, B A D Stocker a
PMCID: PMC235345  PMID: 324978

Abstract

Nearly all of 62 strains of Salmonella paratyphi B were sensitive to colicin M and phage T5 but resistant to phages T1 and ES18 and to colicin B. All tested S. typhimurium strains were resistant to colicin M and phage T5, and many were sensitive to phage ES18. A rough S. typhimurium LT2 strain given the tonA region of Escherichia coli or S. paratyphi B became sensitive to colicin M and phage T5. We infer that the tonA allele of S. paratyphi B, like that of E. coli, determines an outer membrane protein that adsorbs T5 and colicin M but not phage ES18, whereas the S. typhimurium allele determines a protein able to adsorb only ES18. The partial T1 sensitivity of a rough LT2 strain with a tonA allele from E. coli or S. paratyphi B and also the tonB+ phentotype of an E. coli B trp-tonB Δ mutant carrying an F′ trp of LT2 origin showed that S. typhimurium LT2 has a tonB allele like that of E. coli with respect to determination of sensitivity to colicins and phage T1. Rough S. paratyphi B, although T5 sensitive, remained resistant to T1 even when given F′ tonB+ of E. coli origin. Classes of Salmonella mutants selected as resistant to colicin M included: T5-resistant mutants, probably tonA; mutants unchanged except for M resistance, perhaps tolerant; and Exb+ mutants, producing a colicin inhibitor (presumably enterochelin). Some Exb+ mutants were resistant to a bacteriocin inactive on E. coli but active on all tested S. paratyphi B and S. typhimurium strains (and on nearly all other tested Salmonella). A survey showed sensitivity to colicin M in several other species of Salmonella.

Full text

PDF
1216

Selected References

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

  1. Atkinson N. Salmonella antibiotics. 1. Salmonellin, a new colicin-like antibiotic. Aust J Exp Biol Med Sci. 1966 Oct;44(5):559–573. [PubMed] [Google Scholar]
  2. Atkinson N. [Colicin-like antibiotics and bacteriophages of Salmonellas]. Aust J Exp Biol Med Sci. 1970 Apr;48(2):199–206. doi: 10.1038/icb.1970.19. [DOI] [PubMed] [Google Scholar]
  3. Bachmann B. J., Low K. B., Taylor A. L. Recalibrated linkage map of Escherichia coli K-12. Bacteriol Rev. 1976 Mar;40(1):116–167. doi: 10.1128/br.40.1.116-167.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bassford P. J., Jr, Bradbeer C., Kadner R. J., Schnaitman C. A. Transport of vitamin B12 in tonB mutants of Escherichia coli. J Bacteriol. 1976 Oct;128(1):242–247. doi: 10.1128/jb.128.1.242-247.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Braun V., Schaller K., Wolff H. A common receptor protein for phage T5 and colicin M in the outer membrane of Escherichia coli B. Biochim Biophys Acta. 1973 Sep 27;323(1):87–97. doi: 10.1016/0005-2736(73)90433-1. [DOI] [PubMed] [Google Scholar]
  6. Corwin L. M., Fanning G. R., Feldman F., Margolin P. Mutation leading to increased sensitivity to chromium in Salmonella typhimurium. J Bacteriol. 1966 Apr;91(4):1509–1515. doi: 10.1128/jb.91.4.1509-1515.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davies J. K., Reeves P. Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group B. J Bacteriol. 1975 Jul;123(1):96–101. doi: 10.1128/jb.123.1.96-101.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Denney R. M., Yanofsky C. Isolation and characterization of specialized phi80 transducing phages carrying regions of the Salmonella typhimurium trp operon. J Bacteriol. 1974 May;118(2):505–513. doi: 10.1128/jb.118.2.505-513.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dhillon T. S., Dhillon E. K. Studies on bacteriophage distribution. II. Isolation and host rage based classification of phages active on three species of Enterobacteriaceae. Jpn J Microbiol. 1972 Jul;16(4):297–306. doi: 10.1111/j.1348-0421.1972.tb00662.x. [DOI] [PubMed] [Google Scholar]
  10. FREDERICQ P. Recherches sur l'origine des mutants de E. coli V produisant la colicine M. C R Seances Soc Biol Fil. 1951 Jun;145(11-12):930–933. [PubMed] [Google Scholar]
  11. Fredericq P., Smarda J. Complexité du facteur colicinogène B. Ann Inst Pasteur (Paris) 1970 Jun;118(6):767–774. [PubMed] [Google Scholar]
  12. Frost G. E., Rosenberg H. Relationship between the tonB locus and iron transport in Escherichia coli. J Bacteriol. 1975 Nov;124(2):704–712. doi: 10.1128/jb.124.2.704-712.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. GRATIA J. P. R'ESISTANCE 'A LA COLICINE B CHEZ E. COLI. RELATIONS DE SP'ECIFICIT'E ENTRE COLICINES B, I ET V ET PHAGE T-4. ETUDE G'EN'ETIQUE. Ann Inst Pasteur (Paris) 1964 Nov;107:SUPPL–SUPPL:151. [PubMed] [Google Scholar]
  14. Guterman S. K. Colicin B: mode of action and inhibition by enterochelin. J Bacteriol. 1973 Jun;114(3):1217–1224. doi: 10.1128/jb.114.3.1217-1224.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Guterman S. K., Dann L. Excretion of enterochelin by exbA and exbB mutants of Escherichia coli. J Bacteriol. 1973 Jun;114(3):1225–1230. doi: 10.1128/jb.114.3.1225-1230.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Guterman S. K., Luria S. E. Escherichia coli: strains that excrete an inhibitor of colicin B. Science. 1969 Jun 20;164(3886):1414–1414. doi: 10.1126/science.164.3886.1414. [DOI] [PubMed] [Google Scholar]
  17. Hantke K., Braun V. Membrane receptor dependent iron transport in Escherichia coli. FEBS Lett. 1975 Jan 1;49(3):301–305. doi: 10.1016/0014-5793(75)80771-x. [DOI] [PubMed] [Google Scholar]
  18. Jones R. T., Koeltzow D. E., Stocker B. A. Genetic transfer of Salmonella typhimurium and Escherichia coli lipopolysaccharide antigens to Escherichia coli K-12. J Bacteriol. 1972 Sep;111(3):758–770. doi: 10.1128/jb.111.3.758-770.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kuo T. T., Stocker B. A. ES18, a general transducing phage for smooth and nonsmooth Salmonella typhimurium. Virology. 1970 Nov;42(3):621–632. doi: 10.1016/0042-6822(70)90308-9. [DOI] [PubMed] [Google Scholar]
  20. Le Minor L., Chalon A. M. Sensibilité au bactériophage ES18 de cultures de Salmonella dublin, S. enteritidis et S. blegdam et de sérotypes apparentés. Ann Microbiol (Paris) 1975 Apr;126(3):327–331. [PubMed] [Google Scholar]
  21. Low K. B. Escherichia coli K-12 F-prime factors, old and new. Bacteriol Rev. 1972 Dec;36(4):587–607. doi: 10.1128/br.36.4.587-607.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Luckey M., Pollack J. R., Wayne R., Ames B. N., Neilands J. B. Iron uptake in Salmonella typhimurium: utilization of exogenous siderochromes as iron carriers. J Bacteriol. 1972 Sep;111(3):731–738. doi: 10.1128/jb.111.3.731-738.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. MATSUSHIRO A. Specialized transduction of tryptophan markers in Escherichia coli K12 by bacteriophage phi-80. Virology. 1963 Apr;19:475–482. doi: 10.1016/0042-6822(63)90041-2. [DOI] [PubMed] [Google Scholar]
  24. Mäkelä P. H., Ziegler L. An F' episome of Salmonella abony. Acta Pathol Microbiol Scand. 1966;67(4):547–554. doi: 10.1111/apm.1966.67.4.547. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Press R., Glansdorff N., Miner P., De Vries J., Kadner R., Maas W. K. Isolation of transducing particles of phi-80 bacteriophage that carry different regions of the Escherichia coli genome. Proc Natl Acad Sci U S A. 1971 Apr;68(4):795–798. doi: 10.1073/pnas.68.4.795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Pugsley A. P., Reeves P. Iron uptake in colicin B-resistant mutants of Escherichia coli K-12. J Bacteriol. 1976 Jun;126(3):1052–1062. doi: 10.1128/jb.126.3.1052-1062.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rundell K., Shuster C. W. Membrane-associated nucleotide sugar reactions: influence of mutations affecting lipopolysaccharide on the first enzyme of O-antigen synthesis. J Bacteriol. 1975 Sep;123(3):928–936. doi: 10.1128/jb.123.3.928-936.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. STOCKER B. A. Transduction of flagellar characters in Salmonella. J Gen Microbiol. 1953 Dec;9(3):410–433. doi: 10.1099/00221287-9-3-410. [DOI] [PubMed] [Google Scholar]
  30. Sanderson K. E., Hall C. A. F-prime factors of Salmonella typhimurium and an inversion between S. typhimurium and Escherichia coli. Genetics. 1970 Feb;64(2):215–228. doi: 10.1093/genetics/64.2.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sanderson K. E. Linkage map of Salmonella typhimurium, edition IV. Bacteriol Rev. 1972 Dec;36(4):558–586. doi: 10.1128/br.36.4.558-586.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sanderson K. E., Ross H., Ziegler L., Mäkelä P. H. F + , Hfr, and F' strains of Salmonella typhimurium and Salmonella abony. Bacteriol Rev. 1972 Dec;36(4):608–637. doi: 10.1128/br.36.4.608-637.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Wang C. C., Newton A. An additional step in the transport of iron defined by the tonB locus of Escherichia coli. J Biol Chem. 1971 Apr 10;246(7):2147–2151. [PubMed] [Google Scholar]
  34. Wang C. C., Newton A. Iron transport in Escherichia coli: relationship between chromium sensitivity and high iron requirement in mutants of Escherichia coli. J Bacteriol. 1969 Jun;98(3):1135–1141. doi: 10.1128/jb.98.3.1135-1141.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wayne R., Neilands J. B. Evidence for common binding sites for ferrichrome compounds and bacteriophage phi 80 in the cell envelope of Escherichia coli. J Bacteriol. 1975 Feb;121(2):497–503. doi: 10.1128/jb.121.2.497-503.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wilkinson R. G., Gemski P., Jr, Stocker B. A. Non-smooth mutants of Salmonella typhimurium: differentiation by phage sensitivity and genetic mapping. J Gen Microbiol. 1972 May;70(3):527–554. doi: 10.1099/00221287-70-3-527. [DOI] [PubMed] [Google Scholar]
  37. Wilkinson R. G., Stocker B. A. Genetics and cultural properties of mutants of Salmonella typhimurium lacking glucosyl or galactosyl lipopolysaccharide transferases. Nature. 1968 Mar 9;217(5132):955–957. doi: 10.1038/217955a0. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES