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. 1993 Oct;59(10):3418–3423. doi: 10.1128/aem.59.10.3418-3423.1993

Binding of small, acid-soluble spore proteins to DNA plays a significant role in the resistance of Bacillus subtilis spores to hydrogen peroxide.

B Setlow 1, P Setlow 1
PMCID: PMC182468  PMID: 8250563

Abstract

Dormant spores of Bacillus subtilis which lack the majority of the alpha/beta-type small, acid-soluble proteins (SASP) (termed alpha- beta- spores) that coat the DNA in wild-type spores are significantly more sensitive to hydrogen peroxide than are wild-type spores. Hydrogen peroxide treatment of alpha- beta- spores causes DNA strand breaks more readily than does comparable treatment of wild-type spores, and alpha- beta- spores, but not wild-type spores, which survive hydrogen peroxide treatment have acquired a significant number of mutations. The hydrogen peroxide resistance of wild-type spores appears to be acquired in at least two incremental steps during sporulation. The first increment is acquired at about the time of alpha/beta-type SASP synthesis, and the second increment is acquired approximately 2 h later, at about the time of dipicolinic acid accumulation. During sporulation of the alpha- beta- strain, only the second increment of hydrogen peroxide resistance is acquired. In contrast, sporulation mutants which accumulate alpha/beta-type SASP but progress no further in sporulation acquire only the first increment of hydrogen peroxide resistance. These findings strongly suggest that binding of alpha/beta-type SASP to DNA provides one increment of spore hydrogen peroxide resistance. Indeed, binding of alpha/beta-type SASP to DNA in vitro provides strong protection against cleavage of DNA by hydrogen peroxide.

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Selected References

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

  1. Almirón M., Link A. J., Furlong D., Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 1992 Dec;6(12B):2646–2654. doi: 10.1101/gad.6.12b.2646. [DOI] [PubMed] [Google Scholar]
  2. Bayliss C. E., Waites W. M. The effect of hydrogen peroxide on spores of Clostridium bifermentans. J Gen Microbiol. 1976 Oct;96(2):401–407. doi: 10.1099/00221287-96-2-401. [DOI] [PubMed] [Google Scholar]
  3. Errington J., Cutting S. M., Mandelstam J. Branched pattern of regulatory interactions between late sporulation genes in Bacillus subtilis. J Bacteriol. 1988 Feb;170(2):796–801. doi: 10.1128/jb.170.2.796-801.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Fairhead H., Setlow B., Setlow P. Prevention of DNA damage in spores and in vitro by small, acid-soluble proteins from Bacillus species. J Bacteriol. 1993 Mar;175(5):1367–1374. doi: 10.1128/jb.175.5.1367-1374.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fairhead H., Setlow P. Binding of DNA to alpha/beta-type small, acid-soluble proteins from spores of Bacillus or Clostridium species prevents formation of cytosine dimers, cytosine-thymine dimers, and bipyrimidine photoadducts after UV irradiation. J Bacteriol. 1992 May;174(9):2874–2880. doi: 10.1128/jb.174.9.2874-2880.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Goldrick S., Setlow P. Expression of a Bacillus megaterium sporulation-specific gene during sporulation of Bacillus subtilis. J Bacteriol. 1983 Sep;155(3):1459–1462. doi: 10.1128/jb.155.3.1459-1462.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Imlay J. A., Linn S. DNA damage and oxygen radical toxicity. Science. 1988 Jun 3;240(4857):1302–1309. doi: 10.1126/science.3287616. [DOI] [PubMed] [Google Scholar]
  8. Loewen P. C., Switala J. Multiple catalases in Bacillus subtilis. J Bacteriol. 1987 Aug;169(8):3601–3607. doi: 10.1128/jb.169.8.3601-3607.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Mason J. M., Hackett R. H., Setlow P. Regulation of expression of genes coding for small, acid-soluble proteins of Bacillus subtilis spores: studies using lacZ gene fusions. J Bacteriol. 1988 Jan;170(1):239–244. doi: 10.1128/jb.170.1.239-244.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Mason J. M., Setlow P. Essential role of small, acid-soluble spore proteins in resistance of Bacillus subtilis spores to UV light. J Bacteriol. 1986 Jul;167(1):174–178. doi: 10.1128/jb.167.1.174-178.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Nicholson W. L., Setlow B., Setlow P. Binding of DNA in vitro by a small, acid-soluble spore protein from Bacillus subtilis and the effect of this binding on DNA topology. J Bacteriol. 1990 Dec;172(12):6900–6906. doi: 10.1128/jb.172.12.6900-6906.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Nicholson W. L., Setlow P. Dramatic increase in negative superhelicity of plasmid DNA in the forespore compartment of sporulating cells of Bacillus subtilis. J Bacteriol. 1990 Jan;172(1):7–14. doi: 10.1128/jb.172.1.7-14.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Setlow B., Setlow P. Levels of acetyl coenzyme A, reduced and oxidized coenzyme A, and coenzyme A in disulfide linkage to protein in dormant and germinated spores and growing and sporulating cells of Bacillus megaterium. J Bacteriol. 1977 Nov;132(2):444–452. doi: 10.1128/jb.132.2.444-452.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Setlow B., Sun D., Setlow P. Interaction between DNA and alpha/beta-type small, acid-soluble spore proteins: a new class of DNA-binding protein. J Bacteriol. 1992 Apr;174(7):2312–2322. doi: 10.1128/jb.174.7.2312-2322.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Setlow P. I will survive: protecting and repairing spore DNA. J Bacteriol. 1992 May;174(9):2737–2741. doi: 10.1128/jb.174.9.2737-2741.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Setlow P. Small, acid-soluble spore proteins of Bacillus species: structure, synthesis, genetics, function, and degradation. Annu Rev Microbiol. 1988;42:319–338. doi: 10.1146/annurev.mi.42.100188.001535. [DOI] [PubMed] [Google Scholar]
  17. Singh R. P., Setlow B., Setlow P. Levels of small molecules and enzymes in the mother cell compartment and the forespore of sporulating Bacillus megaterium. J Bacteriol. 1977 Jun;130(3):1130–1138. doi: 10.1128/jb.130.3.1130-1138.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Tovar-Rojo F., Setlow P. Effects of mutant small, acid-soluble spore proteins from Bacillus subtilis on DNA in vivo and in vitro. J Bacteriol. 1991 Aug;173(15):4827–4835. doi: 10.1128/jb.173.15.4827-4835.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Tullius T. D., Dombroski B. A. Hydroxyl radical "footprinting": high-resolution information about DNA-protein contacts and application to lambda repressor and Cro protein. Proc Natl Acad Sci U S A. 1986 Aug;83(15):5469–5473. doi: 10.1073/pnas.83.15.5469. [DOI] [PMC free article] [PubMed] [Google Scholar]

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