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Journal of Bacteriology, August 2003, p. 4305-4314, Vol. 185, No. 15
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.15.4305-4314.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Chill Induction of the SigB-Dependent General Stress Response in Bacillus subtilis and Its Contribution to Low-Temperature Adaptation

Matthias Brigulla,^1,2,3 Tamara Hoffmann,¹ Andrea Krisp,^1,2, Andrea Völker,^1,2,3 Erhard Bremer,¹ and Uwe Völker^1,2,3*

Philipps-University Marburg, Department of Biology, Laboratory for Microbiology, D-35032 Marburg,¹ Max-Planck-Institute for Terrestrial Microbiology, D-35043 Marburg,² Ernst-Moritz-Arndt-University, Medical School, Laboratory for Functional Genomics, D-17487 Greifswald, Germany³

Received 3 March 2003/ Accepted 29 April 2003

A variety of environmental and metabolic cues trigger the transient activation of the alternative transcription factor SigB of Bacillus subtilis, which subsequently leads to the induction of more than 150 general stress genes. This general stress regulon provides nongrowing and nonsporulated cells with a multiple, nonspecific, and preemptive stress resistance. By a proteome approach we have detected the expression of the SigB regulon during continuous growth at low temperature (15°C). Using a combination of Western blot analysis and SigB-dependent reporter gene fusions, we provide evidence for high-level and persistent induction of the sigB operon and the SigB regulon, respectively, in cells continuously exposed to low temperatures. In contrast to all SigB-activating stimuli described thus far, induction by low temperatures does not depend on the positive regulatory protein RsbV or its regulatory phosphatases RsbU and RsbP, indicating the presence of an entirely new pathway for the activation of SigB by chill stress in B. subtilis. The physiological importance of the induction of the general stress response for the adaptation of B. subtilis to low temperatures is emphasized by the observation that growth of a sigB mutant is drastically impaired at 15°C. Inclusion of the compatible solute glycine betaine in the growth medium not only improved the growth of the wild-type strain but rescued the growth defect of the sigB mutant, indicating that the induction of the general stress regulon and the accumulation of glycine betaine are independent means by which B. subtilis cells cope with chill stress.

Present address: Klinikum der Philipps-Universität Marburg, Klinik für Neurologie, Kompetenznetz Parkinson, D-35039 Marburg, Germany.

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