Antioxidant Enzyme Activity in Bacterial Resistance to Nicotine Toxicity by Reactive Oxygen Species

Article

Abstract

We analyzed superoxide dismutase (SOD), catalase (CAT), and ATPase activities in the highly nicotine-degrading strain Pseudomonas sp. HF-1 and two standard strains Escherichia coli and Bacillussubtilis in an attempt to understand antioxidant enzymes in bacteria are produced in response to nicotine, which increases the virulence of the bacteria. Nicotine had different effects on different antioxidant enzymes of different bacteria. SOD plays a more important role in resistance to nicotine stress in E. coli than it does in CAT. Multiple antioxidant enzymes are involved in combating oxidative stress caused by nicotine in Pseudomonas sp. HF-1. The contribution of a particular antioxidant enzyme for protection from nicotine stress varies with the growth phase involved. The inhibition of ATPase in Pseudomonas sp. HF-1 at the stationary phase was enhanced with increasing nicotine concentration, showing a striking dose–response relationship. Nicotine probably affected the metabolism of ATP to some extent. Furthermore, different bacteria possessed distinct SOD isoforms to cope with oxidative stress caused by nicotine.

References

  1. Buurman ET, Johnson KD, Kelly RK, MacCormack K (2006) Different modes of action of naphthyridones in gram-positive and gram-negative bacteria. Antimicrob Agents Chemother 50:385–387. doi:10.1128/AAC.50.1.385-387.2006 CrossRefGoogle Scholar
  2. Diaz PI, Zilm PS, Rogers AH (2000) The response to oxidative stress of Fusobacterium nucleatum grown in continuous culture. FEMS Microbiol Lett 187:31–34. doi:10.1111/j.1574-6968.2000.tb09132.x CrossRefGoogle Scholar
  3. Elkins JG, Hassett DJ, Stewart PS, Schweizer HP, McDermott TR (1999) Protective role of catalase in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide. Appl Environ Microbiol 65:4594–4600Google Scholar
  4. Frederick JR, Elkins JG, Bollinger N, Hassett DJ, McDermott TR (2001) Factors affecting catalase expression in Pseudomonas aeruginosa biofilms and planktonic cells. Appl Environ Microbiol 67:1375–1379. doi:10.1128/AEM.67.3.1375-1379.2001 CrossRefGoogle Scholar
  5. Geckil H, Gencer S, Kahraman H, Erenler SO (2003) Genetic engineering of Enterobacter aerogenes with the vitreoscilla hemoglobin gene: cell growth, survival, and antioxidant enzyme status under oxidative stress. Res Microbiol 154:425–431. doi:10.1016/S0923-2508(03)00083-4 CrossRefGoogle Scholar
  6. Gerlach D, Reichardt W, Vettermann S (1998) Extracellular superoxide dismutase from Streptococcus pyogenes type 12 strain is manganese-dependent. FEMS Microbiol Lett 160:217–224. doi:10.1111/j.1574-6968.1998.tb12914.x CrossRefGoogle Scholar
  7. Hassett DJ, Alsabbagh E, Parvatiyar K et al (2000) A protease-resistant catalase, katA, released upon cell lysis during stationary phase is essential for aerobic survival of a Pseudomonas aeruginosa oxyR mutant at low cell densities. J Bacteriol 182:4557–4563. doi:10.1128/JB.182.16.4557-4563.2000 CrossRefGoogle Scholar
  8. Hidalgo A, Betancor L, Moreno R et al (2004) Thermus thermophilus as a cell factory for the production of a thermophilic Mn-dependent catalase which fails to be synthesized in an active form in Escherichia coli. Appl Environ Microbiol 70:3839–3844. doi:10.1128/AEM.70.7.3839-3844.2004 CrossRefGoogle Scholar
  9. Jung S (2003) Expression level of specifc isozymes of maize catalase mutants influences other antioxidants on norflurazon-induced oxidative stress. Pestic Biochem Phys 75:9–17. doi:10.1016/S0048-3575(03)00017-8 CrossRefGoogle Scholar
  10. Kane JK, Konu Ö, Ma JZ, Li MD (2004) Nicotine coregulates multiple pathways involved in protein modification/degradation in rat brain. Mol Brain Res 132:181–191. doi:10.1016/j.molbrainres.2004.09.010 CrossRefGoogle Scholar
  11. Kang YS, Lee Y, Jung H et al (2007) Overexpressing antioxidant enzymes enhances naphthalene biodegradation in Pseudomonas sp. strain As1. Microbiology 153:3246–3254. doi:10.1099/mic.0.2007/008896-0 CrossRefGoogle Scholar
  12. Kovacic P, Cooksy A (2005) Iminium metabolite mechanism for nicotine toxicity and addiction: oxidative stress and electron transfer. Med Hypotheses 64:104–111. doi:10.1016/j.mehy.2004.03.048 CrossRefGoogle Scholar
  13. Kreiner M, Harvey LM, McNeil B (2002) Oxidative stress response of a recombinant Aspergillus niger to exogenous menadione and H2O2 addition. Enzyme Microb Technol 30:346–353. doi:10.1016/S0141-0229(01)00517-8 CrossRefGoogle Scholar
  14. Lampinent J, Virta M, Karp M (1995) Comparison of gram positive and gram negative bacterial strains cloned with different types of luciferase genes in bioluminescence cytotoxicity tests. Environ Toxicol Water Qual 10:157–166. doi:10.1002/tox.2530100211 CrossRefGoogle Scholar
  15. Loprasert S, Vattanaviboon P, Praituan W, Chamnongpol S, Mongkolsuk S (1996) Regulation of the oxidative stress protective enzymes, catalase and superoxide dismutase in Xanthomonas – a review. Gene 179:33–37. doi:10.1016/S0378-1119(96)00427-1 CrossRefGoogle Scholar
  16. Lü ZM, Min H, Xia Y (2004) The response of Escherichia coli, Bacillus subtilis and Burkholderia cepacia WZ1 to oxidative stress of exposing to quinclorac. J Environ Sci Health B 39:431–441. doi:10.1081/PFC-120035928 CrossRefGoogle Scholar
  17. Novotny TE, Zhao F (1999) Consumption and production waste: another externality of tobacco use. Tob Control 8:75–80CrossRefGoogle Scholar
  18. Park W, Jeon CO, Cadillo H, DeRito C, Madsen EL (2004) Survival of naphthalene-degrading Pseudomonas putida NCIB 9816–4 in naphthalene-amended soils: toxicity of naphthalene and its metabolites. Appl Microbiol Biotechnol 64:429–435. doi:10.1007/s00253-003-1420-6 CrossRefGoogle Scholar
  19. Park W, Peña-Llopis S, Lee Y, Demple B (2006) Regulation of superoxide stress in Pseudomonas putida KT2440 is different from the SoxR paradigm in Escherichia coli. Biochem Biophys Res Commun 34:51–56. doi:10.1016/j.bbrc.2005.12.142 CrossRefGoogle Scholar
  20. Qiao D, Seidler FJ, Slotkin TA (2005) Oxidative mechanisms contributing to the developmental neurotoxicity of nicotine and chlorpyrifos. Toxicol Appl Pharm 206:17–26. doi:10.1016/j.taap.2004.11.003 CrossRefGoogle Scholar
  21. Ruan A, Min H, Peng X, Huang Z (2005) Isolation and characterization of Pseudomonas sp. strain HF-1, capable of degrading nicotine. Res Microbiol 156:700–706. doi:10.1016/j.resmic.2005.02.010 CrossRefGoogle Scholar
  22. Salin ML, McCord JM (1974) Superoxide dismutases in polymorphonuclear leukocytes. J Clin Invest 54:1005–1009. doi:10.1172/JCI107816 CrossRefGoogle Scholar
  23. Suntres ZE (2002) Role of antioxidants in paraquat toxicity. Toxicology 18:65–77. doi:10.1016/S0300-483X(02)00382-7 CrossRefGoogle Scholar
  24. Tang QY, Feng MG (2002) DPS data processing system for practical analysis. Science Press, BeijingGoogle Scholar
  25. Venturi V (2003) Control of rpoS transcription in Escherichia coli and Pseudomonas: why so different? Mol Microbiol 49:1–9. doi:10.1046/j.1365-2958.2003.03547.x CrossRefGoogle Scholar
  26. Wood NJ, Sørensen J (2001) Catalase and superoxide dismutase activity in ammonia-oxidising bacteria. FEMS Microbiol Ecol 38:53–58. doi:10.1111/j.1574-6941.2001.tb00881.x CrossRefGoogle Scholar
  27. Yadwad VB, Kallapur VL, Basalingappa S (1990) Inhibition of gill Na+, K+-ATPase activity in dragonfly larva, Pantala flavesens, by endosulfan. Bull Environ Contam Toxicol 44:585–589. doi:10.1007/BF01700880 CrossRefGoogle Scholar
  28. Yao XH, Min H, Lü ZM (2006) Response of superoxide dismutase, catalase, and ATPase activity in bacteria exposed to acetamiprid. Biomed Environ Sci 19:309–314Google Scholar
  29. Yildiz D, Ercal N, Armstrong DW (1998) Nicotine enantiomers and oxidative stress. Toxicology 130:155–165. doi:10.1016/S0300-483X(98)00105-X CrossRefGoogle Scholar
  30. Zheng M, Wang X, Templeton LJ et al (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562–4570. doi:10.1128/JB.183.15.4562-4570.2001 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.College of Life ScienceZhejiang UniversityHangzhouPeople’s Republic of China

Personalised recommendations