NsrA, a Predicted β-Barrel Outer Membrane Protein Involved in Plant Signal Perception and the Control of Secondary Infection in Sinorhizobium meliloti

• Published in: Journal of bacteriology 2018-06, Vol.200 (11)
• Main Authors: Garnerone, Anne-Marie, Sorroche, Fernando, Zou, Lan, Mathieu-Demazière, Céline, Tian, Chang Fu, Masson-Boivin, Catherine, Batut, Jacques
• Format: Article
• Language: English
• Subjects: Adenylyl Cyclases - genetics; Adenylyl Cyclases - metabolism; Alfalfa; Bacteria; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Bacteriology; Cell surface; Cyclic AMP; Cyclic AMP - metabolism; Cytoplasm; Deactivation; Gene expression; Genes; Host plants; Inactivation; Legumes; Life Sciences; Medicago truncatula - microbiology; Membrane proteins; Membrane Proteins - genetics; Membrane Proteins - metabolism; Models, Biological; Molecular chains; Mutation; Mutualism; Negative feedback; Nodules; Perception; Phenotype; Phenotypes; Predictive control; Protein composition; Proteins; Secondary infection; Signal Transduction; Signaling; Sinorhizobium meliloti; Sinorhizobium meliloti - genetics; Sinorhizobium meliloti - physiology; Spotlight; Symbionts; Symbiosis; Topology; Transcription; Vegetal Biology
• ISSN: 0021-9193; 1098-5530
• DOI: 10.1128/JB.00019-18

An ongoing signal exchange fine-tunes the symbiotic interactions between rhizobia and legumes, ensuring the establishment and maintenance of mutualism. In a recently identified regulatory loop, endosymbiotic exerts negative feedback on root infection in response to unknown plant cues. Upon signal perception, three bacterial adenylate cyclases (ACs) of the inner membrane, namely, CyaD1, CyaD2, and CyaK, synthesize the second messenger cAMP, which, together with the cAMP-dependent Clr transcriptional activator, activates the expression of genes involved in root infection control. The pathway that links signal perception at the surface of the cell to cytoplasmic cAMP production by ACs was thus far unknown. Here we first show that CyaK is the cognate AC for the plant signal, called signal 1, that was observed previously in mature nodule and shoot extracts. We also show that inactivation of the gene immediately upstream of , ( ), which encodes a β-barrel protein of the outer membrane, abolished signal 1 perception , whereas overexpression increased signal 1 responsiveness. Inactivation of the gene abolished all Clr-dependent gene expression in nodules and led to a marked hyperinfection phenotype on plants, similar to that of a triple mutant. We suggest that the NsrA protein acts as the (co)receptor for two signal molecules, signal 1 and a hypothetical signal 1', in mature and young nodules that cooperate in controlling secondary infection in symbiosis. The predicted topology and domain composition of the NsrA protein hint at a mechanism of transmembrane signaling. Symbiotic interactions, especially mutualistic ones, rely on a continuous signal exchange between the symbionts. Here we report advances regarding a recently discovered signal transduction pathway that fine-tunes the symbiotic interaction between and its host plant. We have identified an outer membrane protein of , called NsrA, that transduces plant signals to adenylate cyclases in the inner membrane, thereby triggering a cAMP signaling cascade that controls infection. Besides their relevance for the rhizobium-legume symbiosis, these findings shed light on the mechanisms of signal perception and transduction by adenylate cyclases and transmembrane signaling in bacteria.