A metabolic model of the leaf-associated bacterium Paraburkholderia dioscoreae links the ethylene precursor ACC to core carbon pathways

Paraburkholderia dioscoreae MSB3 T is a novel species with potential agricultural impact, isolated from leaf acumens of the “air potato yam” Dioscorea bulbifera. P. dioscoreae ’s genome encodes a relevant combination of features mediating a beneficial plant-associated lifestyle, and it exhibits significant growth promotion when applied to agriculturally important plants such as tomato. Here, we constructed iPR1691, the first genome-scale metabolic model for P. dioscoreae MSB3, which includes 1,687 reactions, 1,487 metabolites, and 1,691 genes. From an available annotation of P. dioscoreae ’s genome, a draft model was constructed using an automated approach followed by automatic gap-filling on Kbase and was manually curated using constraint-based modeling. The plant growth-promoting effect is related to 1-aminocyclopropane-1-carboxylic acid (ACC), an ethylene precursor in plants, which P. dioscoreae can use as a carbon and nitrogen source. Based on the reactions and genes present in the model, and on various pathways available in the MetaCyc database, a pathway for ACC usage was reconstructed. A sequence comparison against a library of phyllosphere bacterial genomes showed a broad occurrence of the pathway genes in phyllosphere strains. Flux balance analysis was used to validate growth of P. dioscoreae on different substrates, corresponding to diverse conditions of carbon and nitrogen availability. The model provides a representation of bacterial growth on ACC, thus elucidating the biochemical and genetic mechanisms of this plant-bacterial interaction. IMPORTANCE Metabolization of the plant ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) is an important mechanism for plant-associated bacteria to regulate their host’s ethylene status. While previous studies have typically focused on the first step (ACC deaminase) as a metabolic sink, we further investigated the metabolic role of ACC for the bacterium. Our model system is the species Paraburkholderia dioscoreae , isolated from leaf acumens of the “air potato yam” Dioscorea bulbifera and shown to mediate a beneficial plant-associated lifestyle, including significant growth promotion when applied to agriculturally important plants such as tomato. Here, we constructed the first genome-scale metabolic network reconstruction for P. dioscoreae , validated against in vitro growth data. The model incorporates a novel pathway that links ACC to succinate and thus explains the utilization of ACC as a carbon source. Moreover, a sequence similarity search of the pathway genes in a library of phyllosphere bacteria indicates that the pathway is present in several other leaf-associated species.