Null mutations in <i>Sinorhizobium meliloti exoS</i> and <i>chvI</i> demonstrate the importance of this two‐component regulatory system for symbiosis

Bélanger, Louise; Dimmick, Kristin A.; Fleming, Jacquelyn S.; Charles, Trevor C.

doi:10.1111/j.1365-2958.2009.06931.x

Cited by 53 publications

(87 citation statements)

References 74 publications

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“…RirA is a transcriptional repressor that regulates iron acquisition and metabolism genes. ExoS-ChvI and FeuPFeuQ signaling is required for S. meliloti symbiosis (32,34), and work on related pathogenic α-proteobacteria has determined that all three regulators have critical functions during host infection (35)(36)(37).…”

Section: Ncr247 and Other Cationic Peptides Activate Three Regulons Imentioning

confidence: 99%

Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

Penterman

Abo

Nisco

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

139

142

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The α-proteobacterium Sinorhizobium meliloti establishes a chronic intracellular infection during the symbiosis with its legume hosts. Within specialized host cells, S. meliloti differentiates into highly polyploid, enlarged nitrogen-fixing bacteroids. This differentiation is driven by host cells through the production of defensin-like peptides called "nodule-specific cysteine-rich" (NCR) peptides. Recent research has shown that synthesized NCR peptides exhibit antimicrobial activity at high concentrations but cause bacterial endoreduplication at sublethal concentrations. We leveraged synchronized S. meliloti populations to determine how treatment with a sublethal NCR peptide affects the cell cycle and physiology of bacteria at the molecular level. We found that at sublethal levels a representative NCR peptide specifically blocks cell division and antagonizes Z-ring function. Gene-expression profiling revealed that the cell division block was produced, in part, through the substantial transcriptional response elicited by sublethal NCR treatment that affected ∼15% of the genome. Expression of critical cell-cycle regulators, including ctrA, and cell division genes, including genes required for Z-ring function, were greatly attenuated in NCR-treated cells. In addition, our experiments identified important symbiosis functions and stress responses that are induced by sublethal levels of NCR peptides and other antimicrobial peptides. Several of these stress-response pathways also are found in related α-proteobacterial pathogens and might be used by S. meliloti to sense host cues during infection. Our data suggest a model in which, in addition to provoking stress responses, NCR peptides target intracellular regulatory pathways to drive S. meliloti endoreduplication and differentiation during symbiosis.rhizobia-legume | host-microbe interactions

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Section: Ncr247 and Other Cationic Peptides Activate Three Regulons Imentioning

confidence: 99%

Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

Penterman

Abo

Nisco

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

139

142

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“…Homologs of the ChvI/ChvG two-component signal transduction system which regulates several key components of the cell envelope in rhizobia, are required for growth of R. leguminosarum, S. meliloti, and Agrobacterium spp. on complex media (4,17,32). A mutation in a periplasmic protease gene, ctpA, which has been implicated in cell envelope development results in an inability of R. leguminosarum to grow on standard complex media, and the mutant forms large, spherical cells on solid TY after incubation for 24 h (22).…”

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confidence: 99%

Mutation of a Broadly Conserved Operon (RL3499-RL3502) from Rhizobium leguminosarum Biovar viciae Causes Defects in Cell Morphology and Envelope Integrity

et al. 2011

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The bacterial cell envelope is of critical importance to the function and survival of the cell; it acts as a barrier against harmful toxins while allowing the flow of nutrients into the cell. It also serves as a point of physical contact between a bacterial cell and its host. Hence, the cell envelope of Rhizobium leguminosarum is critical to cell survival under both free-living and symbiotic conditions. Transposon mutagenesis of R. leguminosarum strain 3841 followed by a screen to isolate mutants with defective cell envelopes led to the identification of a novel conserved operon (RL3499-RL3502) consisting of a putative moxR-like AAA ؉ ATPase, a hypothetical protein with a domain of unknown function (designated domain of unknown function 58), and two hypothetical transmembrane proteins. Mutation of genes within this operon resulted in increased sensitivity to membranedisruptive agents such as detergents, hydrophobic antibiotics, and alkaline pH. On minimal media, the mutants retain their rod shape but are roughly 3 times larger than the wild type. On media containing glycine or peptides such as yeast extract, the mutants form large, distorted spheres and are incapable of sustained growth under these culture conditions. Expression of the operon is maximal during the stationary phase of growth and is reduced in a chvG mutant, indicating a role for this sensor kinase in regulation of the operon. Our findings provide the first functional insight into these genes of unknown function, suggesting a possible role in cell envelope development in Rhizobium leguminosarum. Given the broad conservation of these genes among the Alphaproteobacteria, the results of this study may also provide insight into the physiological role of these genes in other Alphaproteobacteria, including the animal pathogen Brucella.

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“…The ChvG/ChvI TCS in A. tumefaciens positively regulates a number of acid-inducible genes, including aopB, katA, virB, and virE, leading to the hypothesis that the Agrobacterium ChvG/ChvI acts as a pH sensor that regulates virulence genes in response to the acidic conditions encountered during the early stages of infection (19). In S. meliloti, a number of studies have shown that ExoS and ChvI are required for successful symbiosis with alfalfa, the host legume (2,43,45). The ExoS/ChvI TCS in S. meliloti is required for production of succinoglycan and galactoglucan, the two symbiotically active exopolysaccharides (EPSs) (2,7,43,45).…”

mentioning

confidence: 99%

“…These bacteria are uniquely adapted to survive in the rhizosphere as well as intracellularly within legume plant cells (12). During symbiosis, the cell envelope of rhizobia undergoes significant changes, and several cell envelope components are critical for a successful transition from a free living cell to an intracellular bacteroid (2,4,9,12,43). While significant attention has been focused on characterizing individual cell envelope components in free-living cells and during plant infection, a major challenge moving forward is to elucidate how rhizobia integrate multiple signals from their environment to coordinate an appropriate adaptive response to their cell envelope.…”

mentioning

confidence: 99%

“…The most extensively studied TCS in the Rhizobiaceae are the ChvG/ChvI system from Agrobacterium tumefaciens and the homologous ExoS/ChvI system from Sinorhizobium meliloti, where ChvG (ExoS) is the sensor kinase and ChvI is the response regulator (5,7). These TCSs play important roles in both pathogenic and beneficial host-microbe interactions (2,5,7,8,19,43). Mutation of either chvG or chvI in A. tumefaciens results in avirulence toward several different host plants, including infection of stems of Zinnia elegans and Lycopersicon esculentum and of Bryophyllum daigremontianum leaves (5).…”

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confidence: 99%

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Mutation of the Sensor Kinase chvG in Rhizobium leguminosarum Negatively Impacts Cellular Metabolism, Outer Membrane Stability, and Symbiosis

Vanderlinde

Yost

2012

J Bacteriol

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Two-component signal transduction systems (TCS) are a main strategy used by bacteria to sense and adapt to changes in their environment. In the legume symbiont Rhizobium leguminosarum biovar viciae VF39, mutation of chvG, a histidine kinase, caused a number of pleiotropic phenotypes. ChvG mutants are unable to grow on proline, glutamate, histidine, or arginine as the sole carbon source. The chvG mutant secreted smaller amounts of acidic and neutral surface polysaccharides and accumulated abnormally large amounts of poly-ß-hydroxybutyrate. Mutation of chvG caused symbiotic defects on peas, lentils, and vetch; nodules formed by the chvG mutant were small and white and contained only a few cells that had failed to differentiate into bacteroids. Mutation of chvG also destabilized the outer membrane of R. leguminosarum, resulting in increased sensitivity to membrane stressors. Constitutive expression of ropB, the outer membrane protein-encoding gene, restored membrane stability and rescued the sensitivity phenotypes described above. Similar phenotypes have been described for mutations in other ChvG-regulated genes encoding a conserved operon of unknown function and in the fabXL genes required for synthesis of the lipid A very-long-chain fatty acid, suggesting that ChvG is a key component of the envelope stress response in Rhizobium leguminosarum. Collectively, the results of this study demonstrate the important and unique role the ChvG/ChvI TCS plays in the physiology, metabolism, and symbiotic competency of R. leguminosarum.

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Null mutations in Sinorhizobium meliloti exoS and chvI demonstrate the importance of this two‐component regulatory system for symbiosis

Cited by 53 publications

References 74 publications

Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

Mutation of a Broadly Conserved Operon (RL3499-RL3502) from Rhizobium leguminosarum Biovar viciae Causes Defects in Cell Morphology and Envelope Integrity

Mutation of the Sensor Kinase chvG in Rhizobium leguminosarum Negatively Impacts Cellular Metabolism, Outer Membrane Stability, and Symbiosis

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