Abstract
Rhizobia are soil bacteria able to establish a nitrogen-fixing symbiosis with legume plants. Both in soil and in planta, rhizobia spend non-growing periods resembling the stationary phase of in vitro-cultured bacteria. The primary objective of this work was to better characterize gene regulation in this biologically relevant growth stage in Sinorhizobium meliloti. By a tap-tag/mass spectrometry approach, we identified five sigma factors co-purifying with the RNA polymerase in stationary phase: the general stress response regulator RpoE2, the heat shock sigma factor RpoH2, and three extra-cytoplasmic function sigma factors (RpoE1, RpoE3 and RpoE4) belonging to the poorly characterized ECF26 subgroup. We then showed that RpoE1 and RpoE4 i) are activated upon metabolism of sulfite-generating compounds (thiosulfate and taurine), ii) display overlapping regulatory activities, iii) govern a dedicated sulfite response by controlling expression of the sulfite dehydrogenase SorT, iv) are activated in stationary phase, likely as a result of endogenous sulfite generation during bacterial growth. We showed that SorT is required for optimal growth of S. meliloti in the presence of sulfite, suggesting that the response governed by RpoE1 and RpoE4 may be advantageous for bacteria in stationary phase either by providing a sulfite detoxification function or by contributing to energy production through sulfite respiration. This paper therefore reports the first characterization of ECF26 sigma factors, the first description of sigma factors involved in control of sulphur metabolism, and the first indication that endogenous sulfite may act as a signal for regulation of gene expression upon entry of bacteria in stationary phase.
Highlights
Bacteria are exposed to many stressful conditions in nature, including nutrient starvation, which can limit their growth for long time periods
Other alternative sigma factors, such as the heat shock sigma factor RpoH or the extracytoplasmic function (ECF) sigma factor RpoE are active at the end of exponential phase and upon entry in stationary phase, respectively, and mainly control the expression of chaperones and proteases involved in folding and degradation of cytoplasmic and secreted proteins, respectively [5,6,7]
To identify S. meliloti sigma factors possibly activated in stationary phase, we pulled down the RNA polymerase (RNAP) by a tap-tag
Summary
Bacteria are exposed to many stressful conditions in nature, including nutrient starvation, which can limit their growth for long time periods. Bacteria have evolved a number of different strategies that make them able to survive these famine periods Those strategies mainly rely on global reorganization of gene expression, resulting in a number of morphological, physiological and metabolic changes, some of which confer multiple stress resistance to the cells and improve their ability to survive on the long term [2]. In Escherichia coli, the master general stress response regulator RpoS is the main sigma factor in charge of gene expression in stationary phase, as it controls the transcription of several hundreds of genes involved in functions as diverse as acquisition of multiple stress resistance, redirection of metabolism or structuration of the cell envelope [3,4]. Other alternative sigma factors, such as the heat shock sigma factor RpoH or the extracytoplasmic function (ECF) sigma factor RpoE are active at the end of exponential phase and upon entry in stationary phase, respectively, and mainly control the expression of chaperones and proteases involved in folding and degradation of cytoplasmic and secreted proteins, respectively [5,6,7]
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