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Microbiology 148 (2002), 719-726
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Microbiology (2002), 148, 719-726.
© 2002 Society for General Microbiology

Research Paper

The role of two periplasmic copper- and zinc-cofactored superoxide dismutases in the virulence of Salmonella choleraesuis

Assunta Sansone1, Patricia R. Watson2, Timothy S. Wallis2, Paul R. Langford1 and J. Simon Kroll1

Molecular Infectious Diseases Group, Department of Paediatrics, Faculty of Medicine, Imperial College, St Mary’s Hospital Campus, Norfolk Place, London W2 1PG, UK1
Institute for Animal Health, Compton, Newbury, Berkshire, RG20 7NN, UK2

Author for correspondence: J. Simon Kroll. Tel: +44 20 7886 6220. Fax: +44 20 7886 6284. e-mail: s.kroll{at}ic.ac.uk

Periplasmic copper- and zinc-cofactored superoxide dismutases ([Cu,Zn]-SODs, SodC) of several Gram-negative pathogens can protect against superoxide-radical-mediated host defences, and thus contribute to virulence. This role has been previously defined for one [Cu,Zn]-SOD in various Salmonella serovars. Following the recent discovery of a second periplasmic [Cu,Zn]-SOD in Salmonella, the effect of knockout mutations in one or both of the original sodC-1 and the new sodC-2 on the virulence of the porcine pathogen Salmonella choleraesuis is investigated here. In comparison to wild-type, while sodC mutants – whether single or double – showed no impairment in growth, they all showed equally enhanced sensitivity to superoxide and a dramatically increased sensitivity to the combination of superoxide and nitric oxide in vitro. This observation had its correlate in experimental infection both ex vivo and in vivo. Mutation of sodC significantly impaired survival of S. choleraesuis in interferon {gamma}-stimulated murine macrophages compared to wild-type organisms, and all S. choleraesuis sodC mutants persisted in significantly lower numbers than wild-type in BALB/c (Itys) and C3H/HeN (Ityr) mice after experimental infection, but in no experimental system were sodC-1 sodC-2 double mutants more attenuated than either single mutant. These data suggest that both [Cu,Zn]-SODs are needed to protect bacterial periplasmic or membrane components. While SodC plays a role in S. choleraesuis virulence, the data presented here suggest that this is through overcoming a threshold effect, probably achieved by acquisition of sodC-1 on a bacteriophage. Loss of either sodC gene confers maximum vulnerability to superoxide on S. choleraesuis.

Keywords: Superoxide dismutase, Salmonella, periplasm, bacterial [Cu,Zn]-SOD, bacterial virulence

Abbreviations: [Cu,Zn]-SOD, copper- and zinc-cofactored superoxide dismutase; DEDC, diethyldithiocarbamate; FCS, foetal calf serum; IFN{gamma}, interferon {gamma}; i.p., intraperitoneal; ROI/RNI, reactive oxygen/nitrogen intermediate; SOD, superoxide dismutase; SPER/NO, 2,2'-hydroxy-nitrosohydrazono bis-ethanamine (spermine NONOate); X, xanthine; XO, xanthine oxidase




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