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Transcriptomic and metabolic responses of Staphylococcus aureus exposed to supra-physiological temperatures

Fleury, Benedicte
Gotz, Friedrich
Proctor, R. A.
Published in BMC Microbiology. 2009, vol. 9, p. 76
Abstract BACKGROUND: Previous evaluation by different molecular and physiological assays of Staphylococcus aureus (S. aureus) responses to heat shock exposure yielded a still fragmentary view of the mechanisms determining bacterial survival or death at supra-physiological temperatures. This study analyzed diverse facets of S. aureus heat-shock adjustment by recording global transcriptomic and metabolic responses of bacterial cultures shifted for 10 min from 37 degrees C to a sub-lethal (43 degrees C) or eventually lethal (48 degrees C) temperature. A relevant metabolic model of the combined action of specific stress response mechanisms with more general, energy-regulating metabolic pathways in heat-shocked S. aureus is presented. RESULTS: While S. aureus cultures shifted to 43 degrees C or left at 37 degrees C showed marginal differences in growth and survival rates, bacterial cultures exposed to 48 degrees C showed a rapid growth arrest followed by a subsequent decline in viable counts. The most substantial heat shock-induced changes at both 43 degrees C and 48 degrees C occurred in transcript levels of HrcA- and CtsR-regulated genes, encoding classical chaperones DnaK and GroESL, and some Hsp100/Clp ATPases components, respectively. Other metabolic pathways up-regulated by S. aureus exposure at 48 degrees C included genes encoding several enzymes coping with oxidative stress, and DNA damage, or/and impaired osmotic balance. Some major components of the pentose phosphate cycle and gluconeogenesis were also up-regulated, which reflected depletion of free glucose by bacterial cultures grown in Mueller-Hinton broth prior to heat shock. In contrast, most purine- and pyrimidine-synthesis pathway components and amino acyl-tRNA synthetases were down-regulated at 48 degrees C, as well as arginine deiminase and major fermentative pathway components, such as alcohol, lactate and formate dehydrogenases. Despite the heat-induced, increased requirements for ATP-dependent macromolecular repair mechanisms combined with declining energy sources, intracellular ATP levels remained remarkably constant during heat shock. CONCLUSION: The sequential loss of replication and viability at 48 degrees C cannot be explained by significant reductions in intracellular ATP levels, but may reflect ATP rerouting for macromolecular repair mechanisms and cell survival. Our metabolic model also suggests that heat-stressed S. aureus should down-regulate the production of potential, DNA-damaging reactive oxygen species that might result from electron transport-generated ATP, involving excessive levels of free heavy metals, in particular iron.
Keywords Adenosine Triphosphate/metabolismCulture MediaGene Expression ProfilingGene Expression Regulation, BacterialHeat-Shock Response/ geneticsHot TemperatureMetabolomeOligonucleotide Array Sequence AnalysisRNA, Bacterial/metabolismReactive Oxygen Species/metabolismStaphylococcus aureus/ genetics/growth & development/ metabolism
PMID: 19386094
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Research group Acquisition et expression de facteurs de virulence chez Staphylococcus aureus (86)
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FLEURY, Benedicte et al. Transcriptomic and metabolic responses of Staphylococcus aureus exposed to supra-physiological temperatures. In: BMC Microbiology, 2009, vol. 9, p. 76. https://archive-ouverte.unige.ch/unige:9321

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Deposited on : 2010-07-12

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