Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Nov;179(21):6831–6836. doi: 10.1128/jb.179.21.6831-6836.1997

Catalase-peroxidase of Caulobacter crescentus: function and role in stationary-phase survival.

H M Steinman 1, F Fareed 1, L Weinstein 1
PMCID: PMC179615  PMID: 9352936

Abstract

Caulobacter crescentus is an obligate aerobe which is exposed to high concentrations of photosynthetic oxygen and low levels of nutrients in its aquatic environment. Physiological studies of oxidative and starvation stresses in C. crescentus were undertaken through a study of lacZ fusion and null mutant strains constructed from the cloned 5' end of katG, encoding a catalase-peroxidase. The katG gene was shown to be solely responsible for catalase and peroxidase activity in C. crescentus. Like the katG of Escherichia coli, C. crescentus katG is induced by hydrogen peroxide and is important in sustaining the exponential growth rate. However, dramatic differences are seen in growth stage induction. E. coli KatE catalase and KatG catalase-peroxidase activities are induced 15- to 20-fold during exponential growth and then approximately halved in the stationary phase. In contrast, C. crescentus KatG activity is constant throughout exponential growth and is induced 50-fold in the stationary phase. Moreover, the survival of a C. crescentus katG null mutant is reduced by more than 3 orders of magnitude after 24 h in stationary phase and more than 6 orders of magnitude after 48 h, a phenotype not seen for E. coli katE and katG null mutants. These results indicate a major role for C. crescentus catalase-peroxidase in stationary-phase survival and raise questions about whether the peroxidatic activity as well as the protective catalatic activity of the dual-function enzyme is important in the response to starvation stress.

Full Text

The Full Text of this article is available as a PDF (586.7 KB).

Selected References

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

  1. Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121–126. doi: 10.1016/s0076-6879(84)05016-3. [DOI] [PubMed] [Google Scholar]
  2. Alley M. R., Gomes S. L., Alexander W., Shapiro L. Genetic analysis of a temporally transcribed chemotaxis gene cluster in Caulobacter crescentus. Genetics. 1991 Oct;129(2):333–341. doi: 10.1093/genetics/129.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Claiborne A., Fridovich I. Purification of the o-dianisidine peroxidase from Escherichia coli B. Physicochemical characterization and analysis of its dual catalatic and peroxidatic activities. J Biol Chem. 1979 May 25;254(10):4245–4252. [PubMed] [Google Scholar]
  4. Colombi D., Gomes S. L. An alkB gene homolog is differentially transcribed during the Caulobacter crescentus cell cycle. J Bacteriol. 1997 May;179(10):3139–3145. doi: 10.1128/jb.179.10.3139-3145.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Demple B., Halbrook J. Inducible repair of oxidative DNA damage in Escherichia coli. Nature. 1983 Aug 4;304(5925):466–468. doi: 10.1038/304466a0. [DOI] [PubMed] [Google Scholar]
  6. Ely B. Genetics of Caulobacter crescentus. Methods Enzymol. 1991;204:372–384. doi: 10.1016/0076-6879(91)04019-k. [DOI] [PubMed] [Google Scholar]
  7. Evinger M., Agabian N. Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J Bacteriol. 1977 Oct;132(1):294–301. doi: 10.1128/jb.132.1.294-301.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. González-Flecha B., Demple B. Homeostatic regulation of intracellular hydrogen peroxide concentration in aerobically growing Escherichia coli. J Bacteriol. 1997 Jan;179(2):382–388. doi: 10.1128/jb.179.2.382-388.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. González-Flecha B., Demple B. Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J Biol Chem. 1995 Jun 9;270(23):13681–13687. doi: 10.1074/jbc.270.23.13681. [DOI] [PubMed] [Google Scholar]
  10. Hochman A., Figueredo A., Wall J. D. Physiological functions of hydroperoxidases in Rhodobacter capsulatus. J Bacteriol. 1992 May;174(10):3386–3391. doi: 10.1128/jb.174.10.3386-3391.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jenkins D. E., Schultz J. E., Matin A. Starvation-induced cross protection against heat or H2O2 challenge in Escherichia coli. J Bacteriol. 1988 Sep;170(9):3910–3914. doi: 10.1128/jb.170.9.3910-3914.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Johnson R. C., Ely B. Isolation of spontaneously derived mutants of Caulobacter crescentus. Genetics. 1977 May;86(1):25–32. doi: 10.1093/genetics/86.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Loewen P. C. Isolation of catalase-deficient Escherichia coli mutants and genetic mapping of katE, a locus that affects catalase activity. J Bacteriol. 1984 Feb;157(2):622–626. doi: 10.1128/jb.157.2.622-626.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Marcinkeviciene J. A., Magliozzo R. S., Blanchard J. S. Purification and characterization of the Mycobacterium smegmatis catalase-peroxidase involved in isoniazid activation. J Biol Chem. 1995 Sep 22;270(38):22290–22295. doi: 10.1074/jbc.270.38.22290. [DOI] [PubMed] [Google Scholar]
  15. Mohr C. D., Jenal U., Shapiro L. Flagellar assembly in Caulobacter crescentus: a basal body P-ring null mutation affects stability of the L-ring protein. J Bacteriol. 1996 Feb;178(3):675–682. doi: 10.1128/jb.178.3.675-682.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mulvey M. R., Switala J., Borys A., Loewen P. C. Regulation of transcription of katE and katF in Escherichia coli. J Bacteriol. 1990 Dec;172(12):6713–6720. doi: 10.1128/jb.172.12.6713-6720.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. POINDEXTER J. S. BIOLOGICAL PROPERTIES AND CLASSIFICATION OF THE CAULOBACTER GROUP. Bacteriol Rev. 1964 Sep;28:231–295. doi: 10.1128/br.28.3.231-295.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Poindexter J. S. The caulobacters: ubiquitous unusual bacteria. Microbiol Rev. 1981 Mar;45(1):123–179. doi: 10.1128/mr.45.1.123-179.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Prentki P., Krisch H. M. In vitro insertional mutagenesis with a selectable DNA fragment. Gene. 1984 Sep;29(3):303–313. doi: 10.1016/0378-1119(84)90059-3. [DOI] [PubMed] [Google Scholar]
  20. Reisenauer A., Mohr C. D., Shapiro L. Regulation of a heat shock sigma32 homolog in Caulobacter crescentus. J Bacteriol. 1996 Apr;178(7):1919–1927. doi: 10.1128/jb.178.7.1919-1927.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schellhorn H. E., Stones V. L. Regulation of katF and katE in Escherichia coli K-12 by weak acids. J Bacteriol. 1992 Jul;174(14):4769–4776. doi: 10.1128/jb.174.14.4769-4776.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schnell S., Steinman H. M. Function and stationary-phase induction of periplasmic copper-zinc superoxide dismutase and catalase/peroxidase in Caulobacter crescentus. J Bacteriol. 1995 Oct;177(20):5924–5929. doi: 10.1128/jb.177.20.5924-5929.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Shapiro L., Losick R. Protein localization and cell fate in bacteria. Science. 1997 May 2;276(5313):712–718. doi: 10.1126/science.276.5313.712. [DOI] [PubMed] [Google Scholar]
  24. St John G., Steinman H. M. Periplasmic copper-zinc superoxide dismutase of Legionella pneumophila: role in stationary-phase survival. J Bacteriol. 1996 Mar;178(6):1578–1584. doi: 10.1128/jb.178.6.1578-1584.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Steinman H. M. Bacteriocuprein superoxide dismutases in pseudomonads. J Bacteriol. 1985 Jun;162(3):1255–1260. doi: 10.1128/jb.162.3.1255-1260.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Steinman H. M., Ely B. Copper-zinc superoxide dismutase of Caulobacter crescentus: cloning, sequencing, and mapping of the gene and periplasmic location of the enzyme. J Bacteriol. 1990 Jun;172(6):2901–2910. doi: 10.1128/jb.172.6.2901-2910.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Storz G., Altuvia S. OxyR regulon. Methods Enzymol. 1994;234:217–223. doi: 10.1016/0076-6879(94)34088-9. [DOI] [PubMed] [Google Scholar]
  28. Triggs-Raine B. L., Doble B. W., Mulvey M. R., Sorby P. A., Loewen P. C. Nucleotide sequence of katG, encoding catalase HPI of Escherichia coli. J Bacteriol. 1988 Sep;170(9):4415–4419. doi: 10.1128/jb.170.9.4415-4419.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Welinder K. G. Bacterial catalase-peroxidases are gene duplicated members of the plant peroxidase superfamily. Biochim Biophys Acta. 1991 Nov 15;1080(3):215–220. doi: 10.1016/0167-4838(91)90004-j. [DOI] [PubMed] [Google Scholar]
  30. von Ossowski I., Mulvey M. R., Leco P. A., Borys A., Loewen P. C. Nucleotide sequence of Escherichia coli katE, which encodes catalase HPII. J Bacteriol. 1991 Jan;173(2):514–520. doi: 10.1128/jb.173.2.514-520.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES