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Journal of Bacteriology, August 2008, p. 5279-5290, Vol. 190, No. 15
0021-9193/08/$08.00+0     doi:10.1128/JB.00100-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

The Campylobacter jejuni Thiol Peroxidases Tpx and Bcp Both Contribute to Aerotolerance and Peroxide-Mediated Stress Resistance but Have Distinct Substrate Specificities{triangledown}

John M. Atack,1 Philippa Harvey,2 Michael A. Jones,3 and David J. Kelly1*

Department of Molecular Biology and Biotechnology, University of Sheffield, Firth Court, Western Bank, Sheffield S10 2TN, United Kingdom,1 Institute of Animal Health, Compton, Berkshire RG20 7NN, United Kingdom,2 School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonnington LE12 5RD, United Kingdom3

Received 21 January 2008/ Accepted 22 May 2008

The microaerophilic food-borne pathogen Campylobacter jejuni experiences variable oxygen concentrations during its life cycle, especially during transitions between the external environment and the avian or mammalian gut. Single knockout mutations in either one of two related thiol peroxidase genes, tpx and bcp, resulted in normal microaerobic growth (10% [vol/vol] oxygen) but poorer growth than that of the wild type under high-aeration conditions (21% [vol/vol] oxygen). However, a tpx/bcp double mutant had a severe microaerobic growth defect and did not grow at high aeration in shake flasks. Although the single mutant strains were no more sensitive than the wild-type strains in disc diffusion assays with hydrogen peroxide, organic peroxides, superoxide, or nitrosative stress agents, in all cases the double mutant was hypersensitive. Quantitative cell viability and cellular lipid peroxidation assays indicated some increased sensitivity of the single tpx and bcp mutants to peroxide stress. Protein carbonylation studies revealed that the tpx/bcp double mutant had a higher degree of oxygen- and peroxide-induced oxidative protein damage than did either of the single mutants. An analysis of the peroxidase activity of the purified recombinant enzymes showed that, surprisingly, Tpx reduced only hydrogen peroxide as substrate, whereas Bcp also reduced organic peroxides. Immunoblotting of wild-type cell extracts with Tpx- or Bcp-specific antibodies showed increased abundance of both proteins under high aeration compared to that under microaerobic growth conditions. Taken together, the results suggest that Tpx and Bcp are partially redundant antioxidant enzymes that play an important role in protection of C. jejuni against oxygen-induced oxidative stress.

* Corresponding author. Mailing address: Department of Molecular Biology and Biotechnology, University of Sheffield, Firth Court, Western Bank, Sheffield S10 2TN, United Kingdom. Phone: 44 114 222 4414. Fax: 44 114 272 8697. E-mail: d.kelly{at}sheffield.ac.uk

{triangledown} Published ahead of print on 30 May 2008.

Journal of Bacteriology, August 2008, p. 5279-5290, Vol. 190, No. 15
0021-9193/08/$08.00+0     doi:10.1128/JB.00100-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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