Photolyase confers resistance to UV light but does not contribute to the symbiotic benefit of bioluminescence in Vibrio fischeri ES114.

Emma L Walker, Jeffrey L Bose, Eric V Stabb
Author Information
  1. Emma L Walker: Department of Microbiology, University of Georgia, 828 Biological Sciences, Athens, GA 30602, USA.

Abstract

Recent reports suggest that the selective advantage of bioluminescence for bacteria is mediated by light-dependent stimulation of photolyase to repair DNA lesions. Despite evidence for this model, photolyase mutants have not been characterized in a naturally bioluminescent bacterium, nor has this hypothesis been tested in bioluminescent bacteria under natural conditions. We have now characterized the photolyase encoded by phr in the bioluminescent bacterium Vibrio fischeri ES114. Consistent with Phr possessing photolyase activity, phr conferred light-dependent resistance to UV light. However, upon comparing ES114 to a phr mutant and a dark Delta luxCDABEG mutant, we found that bioluminescence did not detectably affect photolyase-mediated resistance to UV light. Addition of the light-stimulating autoinducer N-3-oxo-hexanoyl homoserine lactone appeared to increase UV resistance, but this was independent of photolyase or bioluminescence. Moreover, although bioluminescence confers an advantage for V. fischeri during colonization of its natural host, Euprymna scolopes, the phr mutant colonized this host to the same level as the wild type. Taken together, our results indicate that at least in V. fischeri strain ES114, the benefits of bioluminescence during symbiotic colonization are not mediated by photolyase, and although some UV resistance mechanism may be coregulated with bioluminescence, we found no evidence that light production benefits cells by stimulating photolyase in this strain.

References

  1. Plasmid. 2005 Sep;54(2):114-34 [PMID: 16122560]
  2. Photochem Photobiol. 2005 Jul-Aug;81(4):807-18 [PMID: 15839753]
  3. Appl Environ Microbiol. 2006 Jan;72(1):802-10 [PMID: 16391121]
  4. J Mol Biol. 1983 Jun 5;166(4):557-80 [PMID: 6345791]
  5. Photochem Photobiol. 1984 Jun;39(6):771-3 [PMID: 6379692]
  6. J Biol Chem. 1990 May 15;265(14):8009-15 [PMID: 2110564]
  7. J Bacteriol. 1990 Jul;172(7):3701-6 [PMID: 2163384]
  8. J Bacteriol. 1990 Nov;172(11):6557-67 [PMID: 2172216]
  9. J Mol Biol. 1990 Oct 5;215(3):403-10 [PMID: 2231712]
  10. Microbiology. 2000 Feb;146 ( Pt 2):283-8 [PMID: 10708366]
  11. J Bacteriol. 2000 Aug;182(16):4578-86 [PMID: 10913092]
  12. Nature. 2000 Aug 3;406(6795):477-83 [PMID: 10952301]
  13. J Mol Evol. 2001 Apr;52(4):321-32 [PMID: 11343128]
  14. J Bioenerg Biomembr. 2001 Aug;33(4):353-63 [PMID: 11710810]
  15. J Appl Genet. 2002;43(3):377-89 [PMID: 12177528]
  16. Methods Enzymol. 2002;358:413-26 [PMID: 12474404]
  17. Appl Environ Microbiol. 2003 Feb;69(2):820-6 [PMID: 12571000]
  18. Lancet. 2003 Mar 1;361(9359):743-9 [PMID: 12620739]
  19. Luminescence. 2003 May-Jun;18(3):140-4 [PMID: 12701089]
  20. Appl Environ Microbiol. 2003 Oct;69(10):5928-34 [PMID: 14532046]
  21. Genome Res. 2003 Dec;13(12):2577-87 [PMID: 14656965]
  22. Science. 1977 Apr 22;196(4288):432-4 [PMID: 850787]
  23. Annu Rev Microbiol. 1977;31:549-95 [PMID: 199107]
  24. Microbiol Rev. 1979 Dec;43(4):496-518 [PMID: 396467]
  25. Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10915-9 [PMID: 1438297]
  26. Arch Microbiol. 1993;159(2):160-7 [PMID: 8439236]
  27. J Bacteriol. 1995 Feb;177(4):1053-8 [PMID: 7860584]
  28. Annu Rev Genet. 1994;28:117-39 [PMID: 7893120]
  29. Photochem Photobiol. 1995 Oct;62(4):615-24 [PMID: 7480148]
  30. Biochemistry. 1995 Dec 12;34(49):15886-9 [PMID: 8519744]
  31. J Gen Physiol. 1951 Jul;34(6):835-52 [PMID: 14850704]
  32. J Biol Chem. 1965 Mar;240:1473-81 [PMID: 14284763]
  33. Biochim Biophys Acta. 2005 Feb 25;1707(1):1-23 [PMID: 15721603]
  34. Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3004-9 [PMID: 15703294]
  35. Science. 2005 Mar 4;307(5714):1459-61 [PMID: 15746425]
  36. Arch Microbiol. 2005 Mar;183(3):203-8 [PMID: 15717160]
  37. Environ Microbiol. 2005 May;7(5):723-36 [PMID: 15819854]
  38. FEMS Microbiol Lett. 2005 Sep 1;250(1):105-10 [PMID: 16040205]

Grants

  1. R01 AI050661/NIAID NIH HHS
  2. R01AI50661/NIAID NIH HHS

MeSH Term

Aliivibrio fischeri
Deoxyribodipyrimidine Photo-Lyase
Luminescent Proteins
Molecular Sequence Data
Photobacterium
Radiation Tolerance
Symbiosis
Ultraviolet Rays

Chemicals

Luminescent Proteins
Deoxyribodipyrimidine Photo-Lyase

Word Cloud

Created with Highcharts 10.0.0bioluminescencephotolyaseresistanceUVphrfischeriES114lightbioluminescentmutantadvantagebacteriamediatedlight-dependentevidencecharacterizedbacteriumnaturalVibriofoundalthoughconfersVcolonizationhoststrainbenefitssymbioticRecentreportssuggestselectivestimulationrepairDNAlesionsDespitemodelmutantsnaturallyhypothesistestedconditionsnowencodedConsistentPhrpossessingactivityconferredHoweveruponcomparingdarkDeltaluxCDABEGdetectablyaffectphotolyase-mediatedAdditionlight-stimulatingautoinducerN-3-oxo-hexanoylhomoserinelactoneappearedincreaseindependentMoreoverEuprymnascolopescolonizedlevelwildtypeTakentogetherresultsindicateleastmechanismmaycoregulatedproductioncellsstimulatingPhotolyasecontributebenefit

Similar Articles

Cited By