Tryptophan-Driven Metabolomic Shift in Acidobacteriaceae Reveals Phytohormones and Antifungal Metabolites

Acidobacteriota is one of the most abundant phyla in soils and has recently attracted attention for its potential role in promoting phytosanitary benefits. The metabolomic capabilities of this phylum remain poorly characterised, with few experimentally confirmed metabolites described. To address these gaps, we combined metabolomic profiling with comparative genomic analysis to explore the functional potential of novel strains within the Acidobacteriaceae family. Genome mining across the phylum for plant-growth-promoting traits revealed the presence and taxon-specific enrichment of genes related to phytohormone production, as well as other genes associated with plant-beneficial microorganisms. When tryptophan was added to the cultivation medium, it triggered a strong metabolic response in the strains, resulting in measurable changes in the production levels of phytohormones such as indole-3-acetic acid and indole-3-pyruvate. Building on these findings, we examined the metabolic reprogramming caused by tryptophan supplementation, which suppressed the growth of phytopathogenic fungi, leading to the identification of malassezindoles and pityriacitrins as active agents. This was confirmed by isolating and elucidating the structure of pityriacitrin B and one of its methyl esters through NMR studies. Overall, these findings shed light on the previously unexplored metabolic potential of the Acidobacteriota phylum, emphasising its ecological importance for phytosanitary applications. ImportanceDespite their ubiquity and genomic diversity, the functional metabolism of members of the Acidobacteriota has largely remained uncharacterised. This study links genomic predictions to experimentally verified metabolomic outputs of Acidobacteriaceae, demonstrating tryptophan-responsive metabolic shifts translating to phytohormones and metabolites suppressing fungal growth. Our work underscores the emerging role of Acidobacteriota as important contributors to soil ecosystem functioning and plant-microbe interactions.