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A consolidated analysis of the physiological and molecular responses induced under acid stress in the legume symbiont model soil bacterium Sinorhizobium meliloti

ABSTRACT: Abiotic stresses disturb and limit nitrogen-fixing symbioses between rhizobia and their host legumes. In particular, the effect of extracellular acidity on rhizobia has been taken as a model example for analysis because of the economic impact and worldwide distribution of these symbionts in agricultural countries. Except for valuable molecular-biological studies on different rhizobia, no consolidated models have been formulated to describe the central physiologic changes that occur in acid-stressed bacteria. We present here an integrated analysis entailing the main cultural, metabolic, and molecular responses of the model bacterium Sinorhizobium meliloti growing under controlled acid stress in a chemostat. A stepwise extracellular acidification of the culture medium had indicated that S. meliloti stopped growing at ca. pH 6.0–6.1. Under such a limiting acid stress the rhizobia increased the O2 consumption per cell by more than 5-fold. This phenotype, together with an increase in the transcripts for several membrane cytochromes, entails a remarkably higher aerobic-respiration rate in acid-stressed rhizobia. Changes in the transcripts encoding enzymes for lipid biosynthesis were also observed, consistent with previous data on rhizobial pH-dependent membrane remodelling. Together with increased energy demands under acidity, proteomic and transcriptomic data revealed that while at pH 7.0 the transport and biosynthesis of cellular compounds were quite active processes, under acid stress most overexpressed markers were associated with protein biosynthesis, macromolecular degradation and/or recycling, and energy metabolism. Within this context, the pentose-phosphate pathway exhibited increases in several transcripts, enzymes, and metabolites. Moreover, multivariate analysis of global metabolome data (more than 60 compounds) served to unequivocally correlate the specific-metabolite profiles with the extracellular pH for growth, with strikingly sensitive variations being observed in the rhizobial metabolomes upon extracellular-pH changes of less than 0.5 units. Except for a ca. 120-kb DNA stretch within the pSymA no specific genomic regions were associated with the observed acid-stress responses. Further practical analyses should be focussed on the phenotypic impact and time course of the observed changes during the acid-stress perception and on the search for common responses during the previously described sublethal acid-adaptive processes in rhizobia

ORGANISM(S): Sinorhizobium meliloti 1021 Sinorhizobium meliloti

PROVIDER: GSE74449 | GEO | 2015/10/29

SECONDARY ACCESSION(S): PRJNA300442

REPOSITORIES: GEO

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Project description:Abiotic stresses disturb and limit nitrogen-fixing symbioses between rhizobia and their host legumes. In particular, the effect of extracellular acidity on rhizobia has been taken as a model example for analysis because of the economic impact and worldwide distribution of these symbionts in agricultural countries. Except for valuable molecular-biological studies on different rhizobia, no consolidated models have been formulated to describe the central physiologic changes that occur in acid-stressed bacteria. We present here an integrated analysis entailing the main cultural, metabolic, and molecular responses of the model bacterium Sinorhizobium meliloti growing under controlled acid stress in a chemostat. A stepwise extracellular acidification of the culture medium had indicated that S. meliloti stopped growing at ca. pH 6.0â??6.1. Under such a limiting acid stress the rhizobia increased the O2 consumption per cell by more than 5-fold. This phenotype, together with an increase in the transcripts for several membrane cytochromes, entails a remarkably higher aerobic-respiration rate in acid-stressed rhizobia. Changes in the transcripts encoding enzymes for lipid biosynthesis were also observed, consistent with previous data on rhizobial pH-dependent membrane remodelling. Together with increased energy demands under acidity, proteomic and transcriptomic data revealed that while at pH 7.0 the transport and biosynthesis of cellular compounds were quite active processes, under acid stress most overexpressed markers were associated with protein biosynthesis, macromolecular degradation and/or recycling, and energy metabolism. Within this context, the pentose-phosphate pathway exhibited increases in several transcripts, enzymes, and metabolites. Moreover, multivariate analysis of global metabolome data (more than 60 compounds) served to unequivocally correlate the specific-metabolite profiles with the extracellular pH for growth, with strikingly sensitive variations being observed in the rhizobial metabolomes upon extracellular-pH changes of less than 0.5 units. Except for a ca. 120-kb DNA stretch within the pSymA no specific genomic regions were associated with the observed acid-stress responses. Further practical analyses should be focussed on the phenotypic impact and time course of the observed changes during the acid-stress perception and on the search for common responses during the previously described sublethal acid-adaptive processes in rhizobia pH 6.1 vs pH 7

Project description:Acidic soil disturbs the establishment of the efficient rhizobia commonly used as biofertilizer and the plant-rhizobia interactions. To adapt to different environmental conditions, Sinorhizobium meliloti relies on a complex and finely tuned regulatory network. Although parts of this network have been well-elucidated, most S. meliloti transcriptional regulators remain unexplored. We recently reported that deletion of the ActJK two-component system renders an acid-vulnerable phenotype in S. meliloti and demonstrated the system's requirement for full bacteroid development and nodule occupancy. To more fully understand the role of ActJ in acid tolerance, the proteomes of wild type S. meliloti 2011 and the isogenic actJ- mutant strain were compared in the presence or absence of acid stress by nanoflow ultrahigh-performance liquid chromatography coupled to mass spectrometry. That analysis demonstrated that proteins related to cell wall, membrane, and envelope biogenesis such as those involved in the synthesis of exopolysaccharides (EPS) were notably enriched in actJ- cells in acid pH. Total EPS quantification supported these findings; revealing that although EPS production was augmented at pH 5.6 in both the actJ- and the parental strain, the lack of ActJ significantly enhanced this difference. Moreover, several efflux pumps were found downregulated in the actJ- strain. Promoter fusion assays suggested that ActJ positively modulated its own expression in acid medium but not at neutrality. Irrespective of the extracellular pH, NtrB -a sensory histidine kinase/phosphatase- and DegP1 -a key serine protease mediating protein quality control in diverse Gram-negative bacteria-, are both differentially expressed when ActJ is absent. Unraveling of ActJK-regulated mechanisms will help to understand how this organism deals with the acid stress naturally encountered in soils, infection threads, and symbiosomes. Results presented here identified several ActJ-regulated genes, highlighting key components of the regulatory network associated with the ActJK two-component system in S. meliloti and that system's role in the response of rhizobia to acid stress.

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A consolidated analysis of the physiological and molecular responses induced under acid stress in the legume symbiont model soil bacterium Sinorhizobium meliloti

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