Sinorhizobium meliloti sigma factors RpoE1 and RpoE4 are activated in stationary phase in response to sulfite

PLoS One. 2012;7(11):e50768. doi: 10.1371/journal.pone.0050768. Epub 2012 Nov 30.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Base Sequence
  • Gene Expression Regulation, Bacterial
  • Mass Spectrometry
  • Promoter Regions, Genetic / genetics
  • Regulon / genetics
  • Sigma Factor / genetics
  • Sigma Factor / metabolism*
  • Sinorhizobium meliloti / genetics
  • Sinorhizobium meliloti / growth & development*
  • Sinorhizobium meliloti / metabolism*
  • Sulfites / metabolism*
  • Taurine / metabolism
  • Thiosulfates / metabolism

Substances

  • Bacterial Proteins
  • Sigma Factor
  • Sulfites
  • Thiosulfates
  • Taurine

Grant support

This work was supported in part by the Département Santé des Plantes et Environnement of INRA. The mass spectrometry analyses were supported, in part, by grants from the Fondation pour la Recherche Médicale (contrat Grands Equipements), the Génopole Toulouse Midi-Pyrénées (program Biologie-Santé) and the Région Midi-Pyrénées. This research was done in the Laboratoire des Interactions Plantes-Microorganismes, part of the Laboratoire d’Excellence (LABEX) entitled TULIP (ANR-10-LABX-41). BB was recipient of a French doctoral fellowship (Ministère de la Recherche et de l’Enseignement Supérieur). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.