Acetylcholine chemotaxis in global bacterial plant pathogens

Abstract

Interactions within the plant holobiont involve a wide diversity of plant- and microbial-derived signals. Bacterial perception of these signals allows directed movement along chemical gradients through chemotaxis, a process that is an important determinant for plant colonization and infection. The quaternary amine acetylcholine is primarily known for its function as a neurotransmitter in mammalian nervous systems, but is emerging as a signal molecule that regulates plant growth, development, and stress resistance. Here, we report that plant pathogenic bacteria of the genera Agrobacterium and Dickeya exhibit strong chemotaxis to acetylcholine. These responses are mediated in Agrobacterium fabrum, Dickeya solani, and Dickeya dadantii by the dCache_1-type ligand binding domain (LBD) containing chemoreceptors AtuA, MkcA, and DdaA, respectively, which recognize acetylcholine with affinities between 19 and 91 µM. These chemoreceptors also recognize additional quaternary amines such as choline, L-carnitine, and betaine. The high-resolution structure of MkcA-LBD of D. solani was solved in complex with choline, which allowed the identification of the molecular determinants of choline and acetylcholine recognition in this chemoreceptor. Functionally, DdaA was found to contribute to competitive colonization fitness in planta. Acetylcholine serves as a nutritional source for A. fabrum, but not for D. solani and D. dadantii, and provides osmoprotective effects in all three phytopathogenic species. Plant-associated bacteria exhibit chemotaxis toward a diversity of key plant signals, and their ability to sense acetylcholine may represent an adaptive strategy to ensure efficient plant infection and manage osmotic stress. Our findings suggest potential co-evolutionary interactions between plants and their associated microbiomes.