Glucose-mediated repression of plant biomass utilization in the white-rot fungus Dichomitus squalens

The extent of carbon catabolite repression (CCR) at a global level is unknown in wood-rotting fungi, which are critical to the carbon cycle and are a source of biotechnological enzymes. CCR occurs in the presence of sufficient concentrations of easily metabolizable carbon sources (e.g. glucose), down-regulating the expression of genes encoding enzymes involved in the breakdown of complex carbon sources. We investigated this phenomenon in the white-rot fungus Dichomitus squalens using transcriptomics and exo-proteomics. In D. squalens cultures, approximately 7% of genes were repressed in the presence of glucose compared to Avicel or xylan alone. The glucose-repressed genes included the essential components for utilization of plant biomass – Carbohydrate Active enZyme (CAZy) and carbon catabolic genes. The majority of polysaccharide degrading CAZy genes were repressed and included activities towards all major carbohydrate polymers present in plant cell walls, while also repression of ligninolytic genes occurred. The transcriptome-level repression of the CAZy genes observed on the Avicel cultures was strongly supported by exo-proteomics. Protease encoding genes were generally not glucose-repressed indicating their likely dominant role in scavenging for nitrogen rather than carbon. The extent of CCR is surprising given that D. squalens rarely experiences high free sugar concentrations in its woody environment and indicates that biotechnological use of D. squalens for modification of plant biomass would benefit from de-repressed or constitutively CAZymes-expressing strains.Importance White-rot fungi are critical to the carbon cycle because they can mineralise all wood components using enzymes that also have biotechnological potential. The occurrence of carbon catabolite repression (CCR) in white-rot fungi is poorly understood. Previously, CCR in wood-rotting fungi has only been demonstrated for a small number of genes. We demonstrated widespread glucose-mediated CCR of plant biomass utilisation in the white-rot fungus D. squalens This indicates that the CCR mechanism has been largely retained even though wood-rotting fungi rarely experience commonly considered CCR conditions in their woody environment. The general lack of repression of genes encoding proteases along with the reduction in secreted CAZymes during CCR suggested that the retention of CCR may be connected with the need to conserve nitrogen use while growing on nitrogen-scarce wood. The widespread repression indicates that de-repressed strains could be beneficial for enzyme production.

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