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Infection and Immunity, February 2004, p. 701-708, Vol. 72, No. 2
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.2.701-708.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Two TonB Systems in Actinobacillus pleuropneumoniae: Their Roles in Iron Acquisition and Virulence

Amanda J. Beddek,¹ Brian J. Sheehan,^1, Janine T. Bossé,¹ Andrew N. Rycroft,² J. Simon Kroll,^1* and Paul R. Langford¹

Molecular Infectious Disease Group, Department of Paediatrics, Faculty of Medicine, St. Mary's Campus, Imperial College London, London W2 1PG,¹ Department of Pathology and Infectious Diseases, The Royal Veterinary College, University of London, North Mymms, Hatfield, Hertfordshire AL9 7TA, United Kingdom²

Received 11 June 2003/ Returned for modification 15 September 2003/ Accepted 5 November 2003

Iron acquisition in vivo by Actinobacillus pleuropneumoniae depends upon a functional TonB system. Tonpitak et al. (W. Tonpitak, S. Thiede, W. Oswald, N. Baltes, and G.-F. Gerlach, Infect. Immun. 68:1164-1170, 2000) have described one such system, associated with tbpBA encoding the transferrin receptor, and here we report a second, termed tonB2. This gene cluster (exbB2-exbD2-tonB2) is highly homologous to those in other Pasteurellaceae, unlike the earlier system described (now termed tonB1), suggesting that it is the indigenous system for this organism. Both tonB2 and tonB1 are upregulated upon iron restriction. TonB2, but not TonB1, was found to be essential for growth in vitro when the sole source of iron was hemin, porcine hemoglobin, or ferrichrome. In the case of iron provided as iron-loaded porcine transferrin, neither tonB mutant was viable. The tonB1 phenotype could be explained by a polar effect of the mutation on transcription of downstream tbp genes. We propose that TonB2 is crucial for the acquisition of iron provided in this form, interacting with accessory proteins of the TonB1 system that have been demonstrated to be necessary by Tonpitak et al. TonB2 appears to play a much more important role in A. pleuropneumoniae virulence than TonB1. In an acute porcine infection model, the tonB2 mutant was found to be highly attenuated, while the tonB1 mutant was not. We hypothesize that acquisition of the tonB1-tbp gene cluster confers a biological advantage through its capacity to utilize transferrin-iron but that TonB1 itself plays little or no part in this process.

Editor: V. J. DiRita

Present address: Intervet UK Ltd., Milton Keynes, Buckinghamshire MK7 7AJ, United Kingdom.

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