Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1989 Jun 15;260(3):803–812. doi: 10.1042/bj2600803

The phototrophic bacterium Rhodopseudomonas capsulata sp108 encodes an indigenous class A beta-lactamase.

J I Campbell 1, S Scahill 1, T Gibson 1, R P Ambler 1
PMCID: PMC1138748  PMID: 2788410

Abstract

The nucleotide sequence of a 2.37 kb DNA fragment derived from cloning a total DNA digest of Rhodopseudomonas capsulata sp108 was determined. The DNA codes for a beta-lactamase, a protein showing sequence similarity to the ampR protein of Enterobacter cloacae and an unidentified open reading frame. Hybridization experiments with a probe carrying DNA from within the beta-lactamase gene suggests a chromosomal location for the coding sequences in strain sp108 and in sp109, a penicillin-sensitive revertant of sp108 in which the enzyme is not inducible. A protein-sequence comparison of the deduced amino acid sequence of the Rps. capsulata beta-lactamase indicates that it is a Class A enzyme and that its sequence can be aligned with those of the characterized beta-lactamases from Staphylococcus aureus, Bacillus licheniformis and the Escherichia coli plasmid (R-TEM enzyme), with only a few insertions or deletions. The corresponding DNA sequence is, however, characteristically rhodopseudomonad, suggesting that it is not a recently transposed gene.

Full text

PDF
812

Images in this article

Selected References

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

  1. Ambler R. P., Meadway R. J. Chemical structure of bacterial penicillinases. Nature. 1969 Apr 5;222(5188):24–26. doi: 10.1038/222024a0. [DOI] [PubMed] [Google Scholar]
  2. Ambler R. P., Meyer T. E., Cusanovich M. A., Kamen M. D. The amino acid sequence of the cytochrome c2 from the phototrophic bacterium Rhodopseudomonas globiformis. Biochem J. 1987 Aug 15;246(1):115–120. doi: 10.1042/bj2460115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ambler R. P., Scott G. K. Partial amino acid sequence of penicillinase coded by Escherichia coli plasmid R6K. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3732–3736. doi: 10.1073/pnas.75.8.3732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ambler R. P. The amino acid sequence of Staphylococcus aureus penicillinase. Biochem J. 1975 Nov;151(2):197–218. doi: 10.1042/bj1510197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ambler R. P. The structure of beta-lactamases. Philos Trans R Soc Lond B Biol Sci. 1980 May 16;289(1036):321–331. doi: 10.1098/rstb.1980.0049. [DOI] [PubMed] [Google Scholar]
  6. Arakawa Y., Ohta M., Kido N., Fujii Y., Komatsu T., Kato N. Close evolutionary relationship between the chromosomally encoded beta-lactamase gene of Klebsiella pneumoniae and the TEM beta-lactamase gene mediated by R plasmids. FEBS Lett. 1986 Oct 20;207(1):69–74. doi: 10.1016/0014-5793(86)80014-x. [DOI] [PubMed] [Google Scholar]
  7. Cartwright S. J., Coulson A. F. Active site of staphylococcal beta-lactamase. Philos Trans R Soc Lond B Biol Sci. 1980 May 16;289(1036):370–372. [PubMed] [Google Scholar]
  8. Chory J., Kaplan S. The in vitro transcription-translation of DNA and RNA templates by extracts of Rhodopseudomonas sphaeroides. Optimization and comparison of template specificity with Escherichia coli extracts and in vivo synthesis. J Biol Chem. 1982 Dec 25;257(24):15110–15121. [PubMed] [Google Scholar]
  9. Daldal F., Cheng S., Applebaum J., Davidson E., Prince R. C. Cytochrome c(2) is not essential for photosynthetic growth of Rhodopseudomonas capsulata. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2012–2016. doi: 10.1073/pnas.83.7.2012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dale J. W., Godwin D., Mossakowska D., Stephenson P., Wall S. Sequence of the OXA2 beta-lactamase: comparison with other penicillin-reactive enzymes. FEBS Lett. 1985 Oct 21;191(1):39–44. doi: 10.1016/0014-5793(85)80989-3. [DOI] [PubMed] [Google Scholar]
  11. Datta N., Kontomichalou P. Penicillinase synthesis controlled by infectious R factors in Enterobacteriaceae. Nature. 1965 Oct 16;208(5007):239–241. doi: 10.1038/208239a0. [DOI] [PubMed] [Google Scholar]
  12. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dideberg O., Charlier P., Wéry J. P., Dehottay P., Dusart J., Erpicum T., Frère J. M., Ghuysen J. M. The crystal structure of the beta-lactamase of Streptomyces albus G at 0.3 nm resolution. Biochem J. 1987 Aug 1;245(3):911–913. doi: 10.1042/bj2450911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Donohue T. J., McEwan A. G., Kaplan S. Cloning, DNA sequence, and expression of the Rhodobacter sphaeroides cytochrome c2 gene. J Bacteriol. 1986 Nov;168(2):962–972. doi: 10.1128/jb.168.2.962-972.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. George D. G., Barker W. C., Hunt L. T. The protein identification resource (PIR). Nucleic Acids Res. 1986 Jan 10;14(1):11–15. doi: 10.1093/nar/14.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Heffron F., McCarthy B. J., Ohtsubo H., Ohtsubo E. DNA sequence analysis of the transposon Tn3: three genes and three sites involved in transposition of Tn3. Cell. 1979 Dec;18(4):1153–1163. doi: 10.1016/0092-8674(79)90228-9. [DOI] [PubMed] [Google Scholar]
  17. Herzberg O., Moult J. Bacterial resistance to beta-lactam antibiotics: crystal structure of beta-lactamase from Staphylococcus aureus PC1 at 2.5 A resolution. Science. 1987 May 8;236(4802):694–701. doi: 10.1126/science.3107125. [DOI] [PubMed] [Google Scholar]
  18. Honoré N., Nicolas M. H., Cole S. T. Inducible cephalosporinase production in clinical isolates of Enterobacter cloacae is controlled by a regulatory gene that has been deleted from Escherichia coli. EMBO J. 1986 Dec 20;5(13):3709–3714. doi: 10.1002/j.1460-2075.1986.tb04704.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hu N., Messing J. The making of strand-specific M13 probes. Gene. 1982 Mar;17(3):271–277. doi: 10.1016/0378-1119(82)90143-3. [DOI] [PubMed] [Google Scholar]
  20. Kelly J. A., Dideberg O., Charlier P., Wery J. P., Libert M., Moews P. C., Knox J. R., Duez C., Fraipont C., Joris B. On the origin of bacterial resistance to penicillin: comparison of a beta-lactamase and a penicillin target. Science. 1986 Mar 21;231(4744):1429–1431. doi: 10.1126/science.3082007. [DOI] [PubMed] [Google Scholar]
  21. Kreitman M. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature. 1983 Aug 4;304(5925):412–417. doi: 10.1038/304412a0. [DOI] [PubMed] [Google Scholar]
  22. Lindberg F., Westman L., Normark S. Regulatory components in Citrobacter freundii ampC beta-lactamase induction. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4620–4624. doi: 10.1073/pnas.82.14.4620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lipman D. J., Pearson W. R. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. doi: 10.1126/science.2983426. [DOI] [PubMed] [Google Scholar]
  24. Meyer T. E., Cusanovich M. A., Kamen M. D. Evidence against use of bacterial amino acid sequence data for construction of all-inclusive phylogenetic trees. Proc Natl Acad Sci U S A. 1986 Jan;83(2):217–220. doi: 10.1073/pnas.83.2.217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Murray N. E., Brammar W. J., Murray K. Lambdoid phages that simplify the recovery of in vitro recombinants. Mol Gen Genet. 1977 Jan 7;150(1):53–61. doi: 10.1007/BF02425325. [DOI] [PubMed] [Google Scholar]
  26. Neugebauer K., Sprengel R., Schaller H. Penicillinase from Bacillus licheniformis: nucleotide sequence of the gene and implications for the biosynthesis of a secretory protein in a Gram-positive bacterium. Nucleic Acids Res. 1981 Jun 11;9(11):2577–2588. doi: 10.1093/nar/9.11.2577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nicolas M. H., Honore N., Jarlier V., Philippon A., Cole S. T. Molecular genetic analysis of cephalosporinase production and its role in beta-lactam resistance in clinical isolates of Enterobacter cloacae. Antimicrob Agents Chemother. 1987 Feb;31(2):295–299. doi: 10.1128/aac.31.2.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Queen C. A vector that uses phage signals for efficient synthesis of proteins in Escherichia coli. J Mol Appl Genet. 1983;2(1):1–10. [PubMed] [Google Scholar]
  29. Richmond M. H., Bennett P. M., Choi C. L., Brown N., Brunton J., Grinsted J., Wallace L. The genetic basis of the spread of beta-lactamase synthesis among plasmid-carrying bacteria. Philos Trans R Soc Lond B Biol Sci. 1980 May 16;289(1036):349–359. doi: 10.1098/rstb.1980.0052. [DOI] [PubMed] [Google Scholar]
  30. Sanger F., Coulson A. R., Barrell B. G., Smith A. J., Roe B. A. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol. 1980 Oct 25;143(2):161–178. doi: 10.1016/0022-2836(80)90196-5. [DOI] [PubMed] [Google Scholar]
  31. Saunders V. A., Saunders J. R., Bennett P. M. Extrachromosomal deoxyribonucleic acid in wild-type and photosynthetically incompetent strains of Rhodopseudomonas spheroides. J Bacteriol. 1976 Mar;125(3):1180–1187. doi: 10.1128/jb.125.3.1180-1187.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sistrom W. R. Transfer of chromosomal genes mediated by plasmid r68.45 in Rhodopseudomonas sphaeroides. J Bacteriol. 1977 Aug;131(2):526–532. doi: 10.1128/jb.131.2.526-532.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  35. Staden R. A computer program to enter DNA gel reading data into a computer. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):499–503. doi: 10.1093/nar/12.1part2.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Staden R. Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Res. 1982 Aug 11;10(15):4731–4751. doi: 10.1093/nar/10.15.4731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Staden R., McLachlan A. D. Codon preference and its use in identifying protein coding regions in long DNA sequences. Nucleic Acids Res. 1982 Jan 11;10(1):141–156. doi: 10.1093/nar/10.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Thatcher D. R. The partial amino acid sequence of the extracellular beta-lactamase I of Bacillus cereus 569/H. Biochem J. 1975 May;147(2):313–326. doi: 10.1042/bj1470313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tipper D. J., Strominger J. L. Mechanism of action of penicillins: a proposal based on their structural similarity to acyl-D-alanyl-D-alanine. Proc Natl Acad Sci U S A. 1965 Oct;54(4):1133–1141. doi: 10.1073/pnas.54.4.1133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tybulewicz V. L., Falk G., Walker J. E. Rhodopseudomonas blastica atp operon. Nucleotide sequence and transcription. J Mol Biol. 1984 Oct 25;179(2):185–214. doi: 10.1016/0022-2836(84)90465-0. [DOI] [PubMed] [Google Scholar]
  41. Waxman D. J., Strominger J. L. Penicillin-binding proteins and the mechanism of action of beta-lactam antibiotics. Annu Rev Biochem. 1983;52:825–869. doi: 10.1146/annurev.bi.52.070183.004141. [DOI] [PubMed] [Google Scholar]
  42. Weaver P. F., Wall J. D., Gest H. Characterization of Rhodopseudomonas capsulata. Arch Microbiol. 1975 Nov 7;105(3):207–216. doi: 10.1007/BF00447139. [DOI] [PubMed] [Google Scholar]
  43. Weil J., Cunningham R., Martin R., 3rd, Mitchell E., Bolling B. Characteristics of lambda p4, a lambda derivative containing 9 per cent excess DNA. Virology. 1972 Nov;50(2):373–380. doi: 10.1016/0042-6822(72)90388-1. [DOI] [PubMed] [Google Scholar]
  44. de Bont J. A., Scholten A., Hansen T. A. Dna-Dna hybridization of Rhodopseudomonas capsulata, Rhodopseudomonas sphaeroides and Rhodopseudomonas sulfidophila strains. Arch Microbiol. 1981 Jan;128(3):271–274. doi: 10.1007/BF00422528. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES