Comparative metabolomics of single-strain and co-cultures of seven Fusarium strains causing Fusarium head blight reveals metabolic modifications induced by strain co-occurrence.

Fusarium Head Blight (FHB) is a devastating fungal disease affecting cereal crops, mainly caused by Fusarium graminearum, Fusarium culmorum, Fusarium poae, Fusarium avenaceum, Fusarium langsethiae, Fusarium sporotrichioides, and Fusarium tricinctum. In addition to inducing yield losses, the previous species are responsible for grain contamination with mycotoxins. Co-occurrence of these species is frequent and driven by fungal interactions that influence disease outcomes. To investigate those interactions, intra- and extracellular metabolomic profiles of one representative strain per FHB species were compared. In total, 932 intracellular and 1170 extracellular metabolites were detected. Strains from F. graminearum, F. culmorum, F. sporotrichioides, and F. tricinctum exhibited the highest number of biomarkers (141, 79, 69, and 58, respectively), whereas fewer than 15 biomarkers were detected for strains of F. avenaceum, F. poae, and F. langsethiae. Tracking these biomarkers in in vitro co-cultures revealed that only those associated with the most abundant strains, F. culmorum followed by F. graminearum, were consistently detected. Comparison of biomarker dynamics between single-strain and co-cultures revealed significant differences in accumulation profiles and concentrations, with some biomarkers showing abundance differences of up to 70-fold. This allowed us to raise several hypotheses, including up- and down-accumulation of some biosynthetic pathways, in addition to detoxification, biotransformation, or cross-feeding mechanisms induced by fungal interactions. This work establishes a first conceptual and methodological framework to study Fusarium interactions through metabolomic profiling of Fusarium co-cultures. It aimed to improve our understanding of the FHB disease process to ultimately mitigate its impact.