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. 1982;1(11):1439–1444. doi: 10.1002/j.1460-2075.1982.tb01335.x

Molecular parasitism in the Escherichia coli-Bdellovibrio bacteriovorus system: translocation of the matrix protein from the host to the parasite outer membrane.

F Guerrini, V Romano, M Valenzi, M Di Giulio, M R Mupo, M Sacco
PMCID: PMC553229  PMID: 6765198

Abstract

During the intracellular maturation in Escherichia coli of the parasite Bdellovibrio bacteriovorus the outer membrane, major protein I of E. coli (i.e., the matrix protein) becomes associated with the outer membrane of the emerging parasite cells. The binding properties of this protein with the outer membrane of the host and of the parasite are identical. An analogous phenomenon also occurs during Bdellovibrio parasitism on Klebsiella pneumoniae and on Salmonella typhimurium. Possible roles for this scavenging action of Bdellovibrio, and similar phenomena in other parasitic systems, are discussed.

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Selected References

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

  1. Althauser M., Samsonoff W. A., Anderson C., Conti S. F. Isolation and preliminary characterization of bacteriophages for Bdellovibrio bacteriovorus. J Virol. 1972 Sep;10(3):516–523. doi: 10.1128/jvi.10.3.516-523.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bloom B. R. Games parasites play: how parasites evade immune surveillance. Nature. 1979 May 3;279(5708):21–26. doi: 10.1038/279021a0. [DOI] [PubMed] [Google Scholar]
  3. Clegg J. A., Smithers S. R., Terry R. J. Concomitant immunity and host antigens associated with schistosomiasis. Int J Parasitol. 1971 May;1(1):43–49. doi: 10.1016/0020-7519(71)90045-2. [DOI] [PubMed] [Google Scholar]
  4. DeMartini M., Inouye M. Interaction between two major outer membrane proteins of Escherichia coli: the matrix protein and the lipoprotein. J Bacteriol. 1978 Jan;133(1):329–335. doi: 10.1128/jb.133.1.329-335.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. DeVay J. E., Adler H. E. Antigens common to hosts and parasites. Annu Rev Microbiol. 1976;30:147–168. doi: 10.1146/annurev.mi.30.100176.001051. [DOI] [PubMed] [Google Scholar]
  6. DiRienzo J. M., Nakamura K., Inouye M. The outer membrane proteins of Gram-negative bacteria: biosynthesis, assembly, and functions. Annu Rev Biochem. 1978;47:481–532. doi: 10.1146/annurev.bi.47.070178.002405. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Hashimoto T., Diedrich D. L., Conti S. F. Isolation of a bacteriophage for Bdellovibrio bacteriovorus. J Virol. 1970 Jan;5(1):97–98. doi: 10.1128/jvi.5.1.97-98.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hespell R. B., Odelson D. A. Metabolism of RNA-ribose by Bdellovibrio bacteriovorus during intraperiplasmic growth on Escherichia coli. J Bacteriol. 1978 Dec;136(3):936–946. doi: 10.1128/jb.136.3.936-946.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  11. Lugtenberg B., Bronstein H., van Selm N., Peters R. Peptidoglycan-associated outer membrane proteins in gammegatine bacteria. Biochim Biophys Acta. 1977 Mar 17;465(3):571–578. doi: 10.1016/0005-2736(77)90274-7. [DOI] [PubMed] [Google Scholar]
  12. Manning P. A., Pugsley A. P., Reeves P. Defective growth functions in mutants of Escherichia coli K12 lacking a major outer membrane protein. J Mol Biol. 1977 Oct 25;116(2):285–300. doi: 10.1016/0022-2836(77)90217-0. [DOI] [PubMed] [Google Scholar]
  13. Matin A., Rittenberg S. C. Kinetics of deoxyribonucleic acid destruction and synthesis during growth of Bdellovibrio bacteriovorus strain 109D on pseudomonas putida and escherichia coli. J Bacteriol. 1972 Sep;111(3):664–673. doi: 10.1128/jb.111.3.664-673.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nelson D. R., Rittenberg S. C. Incorporation of substrate cell lipid A components into the lipopolysaccharide of intraperiplasmically grown Bdellovibrio bacteriovorus. J Bacteriol. 1981 Sep;147(3):860–868. doi: 10.1128/jb.147.3.860-868.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nelson D. R., Rittenberg S. C. Partial characterization of lipid A of intraperiplasmically grown Bdellovibrio bacteriovorus. J Bacteriol. 1981 Sep;147(3):869–874. doi: 10.1128/jb.147.3.869-874.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pritchard M. A., Langley D., Rittenberg S. Effects of methotrexate on intraperiplasmic and axenic growth of Bdellovibrio bacteriovorus. J Bacteriol. 1975 Mar;121(3):1131–1136. doi: 10.1128/jb.121.3.1131-1136.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Rittenberg S. C. Nonidentity of Bdellovibrio bacteriovorus strains 109D and 109J. J Bacteriol. 1972 Jan;109(1):432–433. doi: 10.1128/jb.109.1.432-433.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rittenberg S. C., Shilo M. Early host damage in the infection cycle of Bdellovibrio bacteriovorus. J Bacteriol. 1970 Apr;102(1):149–160. doi: 10.1128/jb.102.1.149-160.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rosenbusch J. P. Characterization of the major envelope protein from Escherichia coli. Regular arrangement on the peptidoglycan and unusual dodecyl sulfate binding. J Biol Chem. 1974 Dec 25;249(24):8019–8029. [PubMed] [Google Scholar]
  20. Rosson R. A., Rittenberg S. C. Regulated breakdown of Escherichia coli deoxyribonucleic acid during intraperiplasmic growth of Bdellovibrio bacteriovorus 109J. J Bacteriol. 1979 Nov;140(2):620–633. doi: 10.1128/jb.140.2.620-633.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schnaitman C. A. Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli. J Bacteriol. 1970 Nov;104(2):890–901. doi: 10.1128/jb.104.2.890-901.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Seidler R. J., Starr M. P. Isolation and characterization of host-independent Bdellovibrios. J Bacteriol. 1969 Nov;100(2):769–785. doi: 10.1128/jb.100.2.769-785.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sher A., Hall B. F., Vadas M. A. Acquisition of murine major histocompatibility complex gene products by schistosomula of Schistosoma mansoni. J Exp Med. 1978 Jul 1;148(1):46–57. doi: 10.1084/jem.148.1.46. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Shilo M., Bruff B. Lysis of Gram-negative bacteria by host-independent ectoparasitic Bdellovibrio bacteriovorus isolates. J Gen Microbiol. 1965 Sep;40(3):317–328. doi: 10.1099/00221287-40-3-317. [DOI] [PubMed] [Google Scholar]
  25. Shilo M. Morphological and physiological aspects of the interaction of Bdellovibrio with host bacteria. Curr Top Microbiol Immunol. 1969;50:174–204. doi: 10.1007/978-3-642-46169-9_6. [DOI] [PubMed] [Google Scholar]
  26. Skurray R. A., Hancock R. E., Reeves P. Con--mutants: class of mutants in Escherichia coli K-12 lacking a major cell wall protein and defective in conjugation and adsorption of a bacteriophage. J Bacteriol. 1974 Sep;119(3):726–735. doi: 10.1128/jb.119.3.726-735.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Starr M. P., Seidler R. J. The Bdellovibros. Annu Rev Microbiol. 1971;25:649–678. doi: 10.1146/annurev.mi.25.100171.003245. [DOI] [PubMed] [Google Scholar]
  28. Taylor R. K., Hall M. N., Enquist L., Silhavy T. J. Identification of OmpR: a positive regulatory protein controlling expression of the major outer membrane matrix porin proteins of Escherichia coli K-12. J Bacteriol. 1981 Jul;147(1):255–258. doi: 10.1128/jb.147.1.255-258.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Thomashow M. F., Rittenberg S. C. Intraperiplasmic growth of Bdellovibrio bacteriovorus 109J: N-deacetylation of Escherichia coli peptidoglycan amino sugars. J Bacteriol. 1978 Sep;135(3):1008–1014. doi: 10.1128/jb.135.3.1008-1014.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Thomashow M. F., Rittenberg S. C. Intraperiplasmic growth of Bdellovibrio bacteriovorus 109J: attachment of long-chain fatty acids to escherichia coli peptidoglycan. J Bacteriol. 1978 Sep;135(3):1015–1023. doi: 10.1128/jb.135.3.1015-1023.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Thomashow M. F., Rittenberg S. C. Intraperiplasmic growth of Bdellovibrio bacteriovorus 109J: solubilization of Escherichia coli peptidoglycan. J Bacteriol. 1978 Sep;135(3):998–1007. doi: 10.1128/jb.135.3.998-1007.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Varon M., Drucker I., Shilo M. Early effects of Bdellovibrio infection on the syntheses of protein and RNA of host bacteria. Biochem Biophys Res Commun. 1969 Oct 22;37(3):518–525. doi: 10.1016/0006-291x(69)90946-2. [DOI] [PubMed] [Google Scholar]
  33. Varon M., Levisohn R. Three-membered parasitic system: a bacteriophage, Bdellovibrio bacteriovorus, and Escherichia coli. J Virol. 1972 Mar;9(3):519–525. doi: 10.1128/jvi.9.3.519-525.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Varon M., Shil M. Interacton of Bdellovibrio bacteriovorus and host bacteria. I. Kinetic studies of attachment and invasion of Escherichia coli B by Bdellovibrio bacteriovorus. J Bacteriol. 1968 Mar;95(3):744–753. doi: 10.1128/jb.95.3.744-753.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. van Alphen W., van Seim N., Lugtenberg B. Pores in the outer membrane of Escherichia coli K12: involvement of proteins b and e in the functioning of pores for nucleotides. Mol Gen Genet. 1978 Feb 7;159(1):75–83. doi: 10.1007/BF00401750. [DOI] [PubMed] [Google Scholar]

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