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Genetics and Molecular Biology |
Department of Biomedical Sciences1 and Department of Microbiology and Immunology2, University of South Alabama, Mobile, AL 36688, USA
Biotechnology Laboratory and Departments of Biochemistry and Microbiology, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z33
Department of Biochemistry, Imperial College of Science, Technology and Medicine, London SW7 2AY, UK4
Author for correspondence: Michael P. Spector. Tel: +1 334 380 2710. Fax: +1 334 380 2711. e-mail: mspector{at}usamail.usouthal.edu
The starvation-stress response (SSR) of Salmonella typhimurium includes gene products necessary for starvation avoidance, starvation survival and virulence for this bacterium. Numerous genetic loci induced during carbon-source starvation and required for the long-term-starvation survival of this bacterium have been identified. The SSR not only protects the cell against the adverse effects of long-term starvation but also provides cross-resistance to other environmental stresses, e.g. thermal challenge (55 °C) or acid-pH challenge (pH 2·8). One carbon-starvation-inducible lac fusion, designated stiA was previously reported to be a 
S-dependent SSR locus that is phosphate-starvation, nitrogen-starvation and H2O2 inducible, positively regulated by (p)ppGpp in a relA-dependent manner, and negatively regulated by cAMP:cAMP receptor protein complex and OxyR. We have discovered through sequence analysis and subsequent biochemical analysis that the stiA::lac fusion, and a similarly regulated lac fusion designated sti-99, lie at separate sites within the first gene (narZ) of an operon encoding a cryptic nitrate reductase (narZYWV) of unknown physiological function. In this study, it was demonstrated that narZ was negatively regulated by the global regulator Fnr during anaerobiosis. Interestingly, narZ(YWV) was required for carbon-starvation-inducible thermotolerance and acid tolerance. In addition, narZ expression was induced ~20-fold intracellularly in Madin-Darby canine kidney epithelial cells and ~16-fold in intracellular salts medium, which is believed to mimic the intracellular milieu. Also, a narZ1 knock-out mutation increased the LD50 ~10-fold for S. typhimurium SL1344 delivered orally in the mouse virulence model. Thus, the previously believed cryptic and constitutive narZYWV operon is in fact highly regulated by a complex network of environmental-stress signals and global regulatory functions, indicating a central role in the physiology of starved and stressed cells.
Keywords: nitrate reductases, stiA, thermotolerance, acid tolerance, starvation-stress response
Abbreviations: CRP, cAMP receptor protein; ISM, intracellular salts medium; LB, Luria–Bertani; MDCK, Madin-Darby canine kidney; MS loPCN, MOPS-buffered salts medium limiting for glucose; MS hiPCN, MOPS-buffered salts medium non-limiting for glucose, phosphate and nitrogen; SP-PCR, single-primer polymerase chain reaction; SSR, starvation-stress response; NR, nitrate reductase
a Present Address: Centro de Biologia Molecular ‘Severo Ochoa’, Universidad Autónoma de Madrid, 28049 Madrid, Spain.
b Present Address: Department of Microbiology and Molecular Genetics, University of California at Los Angeles, Los Angeles, CA 90095, USA.
c Present Address: Microbial Pathogenicity Research Group, Department of Medical Microbiology, St. Bartholomew’s and the Royal London School of Medicine and Dentistry, London EC1A 7BE, UK.
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