Extracellular dGMP enhances Deinococcus radiodurans tolerance to oxidative stress

PLoS One. 2013;8(1):e54420. doi: 10.1371/journal.pone.0054420. Epub 2013 Jan 24.

Abstract

Free extracellular DNA provides nutrition to bacteria and promotes bacterial evolution by inducing excessive mutagenesis of the genome. To understand the influence of extracellular DNA fragments on D. radiodurans, we investigated cell growth and survival after extracellular DNA or dNMPs treatment. The results showed that the extracellular DNA fragments inhibited the growth of D. radiodurans. Interestingly, dGMP, a DNA component, enhanced D. radiodurans tolerance to H(2)O(2) and gamma-radiation significantly. Further experiments indicated that extracellular dGMP stimulated the activity of one catalase (KatA, DR1998), and induced gene transcription including the extracellular nuclease (drb0067). When this only extracellular nuclease gene (drb0067) in D. radiodurans was deleted, the mutant strain showed more sensitive to H(2)O(2) and gamma-radiation than the wild type strain. These results suggest that DRB0067 plays an important role in oxidative stress resistance. Taken together, we proposed a new anti-oxidation mechanism in D. radiodurans. This mechanism acts to increase expression levels of DRB0067 which then secretes active nuclease to degrade extracellular DNA fragments. The extracellular nuclease has a two-fold benefit, creating more free dNTPs for further cell protection and the removal of extracellular DNA fragments.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Catalase / genetics
  • Catalase / metabolism
  • DNA, Bacterial*
  • Deinococcus / drug effects
  • Deinococcus / enzymology*
  • Deinococcus / genetics*
  • Deinococcus / radiation effects
  • Deoxyguanine Nucleotides / pharmacology*
  • Deoxyribonucleases / genetics*
  • Deoxyribonucleases / metabolism
  • Escherichia coli / drug effects
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Escherichia coli / radiation effects
  • Extracellular Space / metabolism
  • Gamma Rays
  • Gene Expression Regulation, Bacterial / drug effects
  • Gene Expression Regulation, Bacterial / radiation effects
  • Hydrogen Peroxide / pharmacology
  • Oxidative Stress / drug effects
  • Oxidative Stress / radiation effects
  • Radiation Tolerance / drug effects
  • Transcription, Genetic / drug effects
  • Transcription, Genetic / radiation effects

Substances

  • Bacterial Proteins
  • DNA, Bacterial
  • Deoxyguanine Nucleotides
  • 2'-deoxyguanosine 5'-phosphate
  • Hydrogen Peroxide
  • Catalase
  • Deoxyribonucleases

Grants and funding

This work was supported by grants from National Natural Science Foundation of China (30830006, 31070080), a major project for genetically modified organisms breeding from the Ministry of Agriculture of China (2009ZX08009-075B, 2011ZX08009-003-002), a grant from Special Fund for Agroscientific Research in the Public Interest from the Ministry of Agriculture of China (201103007), and the Fundamental Research Funds for the Central Universities from Zhejiang University (2012FZA6014). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.