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

Abstract

Chemotaxis to plant compounds is frequently the initial step for the colonization of plants by bacteria. Plant pathogens and plant-associated bacteria contain approximately twice as many chemoreceptors as the bacterial average does, indicating that chemotaxis is particularly important for bacteria–plant interactions. However, information on the corresponding chemoreceptors and their chemoeffectors is limited. We identify the chemoreceptor PacP from the phytopathogen Pectobacterium atrosepticum, which exclusively recognizes phosphorylated C3 compounds at its sCache ligand binding domain, mediating chemoattraction. Using a motif of PacP amino acid residues involved in ligand binding, we identify a chemoreceptor family, termed sCache_PC3, that is specific for phosphorylated C3 compounds. Isothermal titration calorimetry studies reveal that family members preferentially bind glycerol 3-phosphate, a key plant signaling molecule. Family members recognize 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 responds primarily to Krebs cycle intermediates. Members of the sCache_PC3 family are predominantly found in plant-associated bacteria, including many important phytopathogens belonging to the genera Brenneria, Dickeya, Musicola, Pectobacterium, and Herbaspirillum. Consistently, glycerol 3-phosphate is a signal molecule that is excreted by plants in response to stress and infection. Chemotaxis toward glycerol 3-phosphate may be a means for bacteria to localize stressed plants and move to infection sites. This study lays the groundwork for investigating the role of chemotaxis to phosphorylated C3 compounds in plant–bacteria interactions and virulence.