A Sinorhizobium meliloti osmosensory two‐component system required for cyclic glucan export and symbiosis

Abstract

SummaryA screen for novel symbiotic mutants of the nitrogenfixing legume symbiont Sinorhizobium meliloti uncovered a crucial role for the putative response regulator FeuP in the symbiotic infection process. Transcriptome analysis shows that FeuP controls the transcription of at least 16 genes, including ndvA, which encodes an ATP-dependent exporter of cyclic b glucans. Loss of feuP function gives rise to traits associated with cyclic b glucan biosynthetic defects, including poor growth and motility under hypoosmotic conditions, and the inability to invade plant tissue during the early stages of symbiotic infection. Analysis of cyclic glucans indicates that the feuP mutant is able to synthesize intracellular cyclic b glucans, but is unable to export them. Cyclic b glucan export can be restored to feuP mutant cells by constitutive expression of ndvA; likewise, the symbiotic phenotype of a feuP mutant is rescued by ectopic ndvA expression. We further show that the linked sensor kinase gene, feuQ, is also important for modulating ndvA transcription, and that signalling through the FeuP/FeuQ pathway is responsive to extracellular osmotic conditions, with low osmolarity stimulating ndvA expression.

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

“…These twocomponent systems are comprised of a membrane-embedded histidine kinase sensor (ExoS and FeuP) and a cytoplasmic response regulator (ChvI and FeuQ) (32,33). Both ExoS-ChvI and FeuP-FeuQ are critical for S. meliloti symbiosis.…”

“…Both ExoS-ChvI and FeuP-FeuQ are critical for S. meliloti symbiosis. Bacteria with mutations that severely perturb ExoS-ChvI or FeuP-FeuQ signaling produce insufficient levels of exopolysaccharides or cyclic glucans, respectively, and fail to stimulate infection thread growth properly (32,44). Genetic studies on these signaling systems also indicate that they have additional important functions in later stages of the symbiosis (32,45,46).…”

“…Bacteria with mutations that severely perturb ExoS-ChvI or FeuP-FeuQ signaling produce insufficient levels of exopolysaccharides or cyclic glucans, respectively, and fail to stimulate infection thread growth properly (32,44). Genetic studies on these signaling systems also indicate that they have additional important functions in later stages of the symbiosis (32,45,46). In pathogenic bacterial species, two-component systems have evolved to sense AMP activity directly, along with other signals, and activation of these systems leads to changes in gene expression that increase AMP resistance (47).…”

“…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).…”

Genetic analysis of signal integration by the Sinorhizobium meliloti sensor kinase FeuQ

“…The FeuPQ TCS is required for functional symbiotic interaction between Sinorhizobium meliloti and compatible legumes (Griffitts et al, 2008). The FeuPQ regulon consists of at least 16 target genes, including the symbiotically important gene ndvA.…”