Cellular Responses to Quaternary Ammonium Compounds by Pseudomonas Syringae that Influence its Interactions with Plants

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Intellectual Merit Plants are colonized by a diversity of microorganisms, including many that influence plant and environmental health. Plants produce a class of compounds called quaternary ammonium compounds (QACs) that are important to plant membranes and to plant tolerance to drought and salinity stress. These compounds, including betaine, carnitine, and choline, may also benefit plant-associated bacteria. For example, betaine can confer protection to stresses, choline can serve as a building block for some bacterial membrane lipids, and choline-O-sulfate may help store sulfur. Most plant-associated bacteria, including the plant pathogen Pseudomonas syringae, cannot synthesize QACs and thus are dependent on production by the host. Consequently, these organisms have likely evolved mechanisms to import and exploit these compounds. In support of this, the ability to transport choline was recently shown to provide a clear fitness benefit to P. syringae during its colonization of plants. Moreover, studies characterizing the full set of P. syringae transporters for choline and betaine uptake identified additional novel cellular components that may be involved in QAC metabolism and regulation. The goals of this project are to characterize the responses of P. syringae to specific plant-derived QACs and evaluate how these responses influence P. syringae interactions with plants. To address these goals, first, carnitine will be examined as an attractant and nutrient source by investigating the role of a newly identified carnitine-responsive chemotaxis protein in directing bacterial movement to germinating seedlings, and by identifying the genes required for carnitine catabolism and their contribution to fitness. Second, choline-O-sulfate will be evaluated as a source of sulfur and nutrients by characterizing how the loss of transport and catabolism impact P. syringae fitness on plants and by more extensively characterizing the cellular components involved in choline-O-sulfate uptake. And third, betaine, choline, phosphorylcholine and phosphatidylcholine will be evaluated as signal molecules for bacteria by examining global gene expression patterns in P. syringae mutants that lack the ability to degrade individual compounds and thus are able to accumulate them. These studies will significantly advance our understanding of how the perception, signaling and metabolism of this special class of compounds by P. syringae influences the ability of this widely studied bacterial pathogen to colonize plants. Plant-associated P. syringae populations are relevant not only as reservoirs of pathogens for plant disease, but also as reservoirs of biological ice nuclei that may have a role in atmospheric processes leading to rain. Insights into the impact of QACs on leaf-associated bacterial populations are of timely importance because increases in drought, as predicted by global climate change models, and salinity, as is occurring in large areas of irrigated agricultural lands, can result in increased QAC abundance in plant tissues, due to either natural accumulation or agricultural engineering to improve drought and salinity tolerance. Broader Impacts This project will contribute to education by providing training for one graduate student and significant research experiences for at least five undergraduate students, several of which are expected to be members of under-represented groups in the sciences. Outreach activities will provide internships for two biology teachers (7th-12th grade) through an established program at Iowa State University for biology teachers, with the subsequent co-development and implementation of discovery-based curricula based on bacterial ice nucleation and leaf colonization. Outreach activities will also include directing at least two workshops to advance the involvement of middle school students from under-represented groups in the sciences through the Science Bound program at Iowa State University, and co-directing a workshop on plant pathogens for elementary students and their parents.