Adapted Carbon Catabolite Regulation in a Carbohydrate Selective Wood Decomposition Fungus

Abstract:

Wood decomposer fungi evolved carbohydrate-selective manner to only extract carbohydrates embedded in lignin, causing "brown rot" of wood biomass. Brown rot fungi play important roles in recycling the largest pool of above ground carbons sequestered in forest. These fungi contribute to > 80% wood decomposition in boreal system, although they only account ~10% of named wood decay fungi. We now know that brown rot mechanism involves “two-step” gene regulation to first use ROS (reactive oxygen species, e.g., hydroxyl radicals) to break down wood structures and then use cellulase for hydrolysis. We do not know, however, what catabolites and signaling cascades the fungus uses to sense, react, and control this two-step mechanism. Recently, we investigated the genome-wide regulatory responses to carbon catabolites in model brown rot fungus Rhodonia (Postia) placenta. We identified co-regulated gene regulons as shared transcriptional responses to no-carbon controls, glucose, cellobiose, or aspen wood (Populus sp.). We found that cellobiose, a common inducing catabolite for fungi, induced expression of main chain-cleaving cellulases in GH5 and GH12 families (cellobiose vs. no-carbon > 4-fold, P_adj < 0.05), whereas complex aspen was a universal inducer for Carbohydrate Active Enzymes (CAZymes) expression. We also found no glucose-mediated carbon catabolite repression (CCR) for main-chain CAZymes expression, confirming well-known distinction of brown rot fungi from the ancestral counterpart, white rot fungi. Unexpectedly, however, we observed CCR for side-chain cleaving hemicellulases and oxidoreductases, an important discovery that specifically highlights a brown rot fungal adaptation in CAZymes regulation. Using these data, we assembled a network model of this adapted regulatory machinery, built using cis- and trans-elements of carbon regulons. These results offer mechanistic insight into the energy efficiency traits of a common group of decomposer fungi with enormous influence on the carbon cycle.