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Journal of Bacteriology, August 2002, p. 4187-4196, Vol. 184, No. 15
0021-9193/02/$04.00+0     DOI: 10.1128/JB.184.15.4187-4196.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Growth of Campylobacter jejuni Supported by Respiration of Fumarate, Nitrate, Nitrite, Trimethylamine-N-Oxide, or Dimethyl Sulfoxide Requires Oxygen

Michael J. Sellars, Stephen J. Hall, and David J. Kelly*

Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield S10 2TN, United Kingdom

Received 28 November 2001/ Accepted 13 May 2002

The human gastrointestinal pathogen Campylobacter jejuni is a microaerophilic bacterium with a respiratory metabolism. The genome sequence of C. jejuni strain 11168 reveals the presence of genes that encode terminal reductases that are predicted to allow the use of a wide range of alternative electron acceptors to oxygen, including fumarate, nitrate, nitrite, and N- or S-oxides. All of these reductase activities were present in cells of strain 11168, and the molybdoenzyme encoded by Cj0264c was shown by mutagenesis to be responsible for both trimethylamine-N-oxide (TMAO) and dimethyl sulfoxide (DMSO) reduction. Nevertheless, growth of C. jejuni under strictly anaerobic conditions (with hydrogen or formate as electron donor) in the presence of any of the electron acceptors tested was insignificant. However, when fumarate, nitrate, nitrite, TMAO, or DMSO was added to microaerobic cultures in which the rate of oxygen transfer was severely restricted, clear increases in both the growth rate and final cell density compared to what was seen with the control were obtained, indicative of electron acceptor-dependent energy conservation. The C. jejuni genome encodes a single class I-type ribonucleotide reductase (RNR) which requires oxygen to generate a tyrosyl radical for catalysis. Electron microscopy of cells that had been incubated under strictly anaerobic conditions with an electron acceptor showed filamentation due to an inhibition of cell division similar to that induced by the RNR inhibitor hydroxyurea. An oxygen requirement for DNA synthesis can thus explain the lack of anaerobic growth of C. jejuni. The results indicate that strict anaerobiosis is a stress condition for C. jejuni but that alternative respiratory pathways can contribute significantly to energy conservation under oxygen-limited conditions, as might be found in vivo.

* Corresponding author. Mailing address: Department of Molecular Biology and Biotechnology, University of Sheffield, Firth Ct., 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.

Journal of Bacteriology, August 2002, p. 4187-4196, Vol. 184, No. 15
0021-9193/02/$04.00+0     DOI: 10.1128/JB.184.15.4187-4196.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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