Chemoreceptor family in plant-associated bacteria responds preferentially to the plant signal molecule glycerol 3-phosphate

Abstract

Plant pathogens and plant-associated bacteria contain about twice as many chemoreceptors as the bacterial average, indicating that chemotaxis is particularly important for bacteria-plant interactions. However, information on the corresponding chemoreceptors is limited. In this study, we identified the chemoreceptor PacP from the phytopathogen Pectobacterium atrosepticum, which exclusively recognized C3 phosphorylated compounds at its sCache ligand binding domain, mediating chemoattraction. Using a motif of PacP amino acid residues involved in ligand binding, we identified a chemoreceptor family, termed sCache_PC3, that was specific for C3 phosphorylated compounds. Isothermal titration calorimetry studies revealed that family members preferentially bound glycerol 3-phosphate, a key plant signaling molecule. Additionally, family members recognized glycerol 2-phosphate and glycolysis intermediates glyceraldehyde 3-phosphate, dihydroxyacetone phosphate and 3-phosphoglycerate. This study presents the first evidence of chemoreceptors that bind phosphorylated compounds. We show that the sCache_PC3 family has evolved from an ancestral sCache domain that respond primarily to Krebs cycle intermediates. Members of the sCache_PC3 family were mainly found in bacteria that interact with plants, including many important plant pathogens such as Brenneria, Dickeya, Musicola, Pectobacterium, and Herbaspirillum. Glycerol 3-phosphate is a signal molecule that is excreted by plants in response to stress and infection. Chemotaxis towards this molecule may thus be a means for bacteria to localize stressed plants and move to infection sites. This study lays the groundwork for investigating the functional importance of chemotaxis to phosphorylated C3 compounds in plant-bacteria interactions and virulence. Significance statementThe bacterial lifestyle has shaped the evolution of signal transduction systems, and the number and type of chemoreceptors varies greatly between bacteria occupying various ecological niches. Our understanding of the relationship between lifestyle and chemoreceptor function is limited and the discovery of a chemoreceptor family in plant-associated bacteria that primarily responds to an important plant signal molecule is a significant advancement, allowing for further studies to determine its physiological relevance. The lack of knowledge about signals recognized by bacterial receptors is currently a major challenge in microbiology. This study illustrates the potential of combining experimental ligand screening with computational ligand prediction to identify signals recognized by uncharacterized receptors.