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Abstract White-rot fungi are efficient organisms for the mineralization of lignin and polysaccharides into CO2 and H2O. Despite their biotechnological potential, WRF metabolism remains underexplored. Building on recent findings regarding the utilization of lignin-related aromatic compounds as carbon sources by WRF, we aimed to gain further insights into these catabolic processes. For this purpose, Trametes versicolor and Gelatoporia subvermispora were incubated in varying conditions – in static and agitation modes and different antioxidant levels – during the conversion of 4-hydroxybenzoic acid (a lignin-related compound) and cellobiose. Their metabolic responses were assessed via transcriptomics, proteomics, lipidomics, metabolomics, and microscopy analyses. These analyses reveal the significant impact of cultivation conditions on sugar and aromatic catabolic pathways, as well as lipid composition of the fungal mycelia. Additionally, this study identifies biosynthetic pathways for the production of extracellular fatty acids and phenylpropanoids – both products with relevance in biotechnological applications – and provides insights into carbon fate in nature.