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Transcription factor reveals interconnected regulation of carbon source utilization and carbon catabolite repression in an oleaginous yeast

ABSTRACT: Cells must sense and respond to available nutrients to utilize available resources and establish fungal colonies. Saprophytic microbes harvest carbon from plant biomass, which contain insoluble, complex carbohydrates that must be degraded extracellularly prior to import into the cell. Filamentous fungi can degrade these complex carbohydrates. However, while many single cellular microbes can utilize the building blocks of these insoluble polysaccharides, they frequently are unable to degrade insoluble carbohydrates. Cellobiose is a disaccharide breakdown product of cellulose, the most abundant component of plant biomass. We investigated the genetic regulation of cellobiose utilization in the oleaginous, basidiomycete yeast Rhodotorula (Rhodosporidium) toruloides using a combination of phylogenetic, genetic, and genomic approaches. We tested the closest R. toruloides homolog of the cellulose degradation regulator CLR-2/ClrB for a role in cellobiose utilization. Deletion of this transcription factor, which we named Cbr1, eliminated the ability of cells to grow on media containing cellobiose as the sole carbon source. Although, the role of CLR-2/ClrB is limited to regulating the expression of genes involved in the utilization of cellulose and hemicellulose, Cbr1 plays a role not only in cellobiose utilization, but also utilization of tricarboxylic acid (TCA) cycle intermediates. Transcriptional profiling revealed that the genes activated by Cbr1 included genes encoding beta-glucosidases and transporters. These beta-glucosidases are secreted and are necessary and sufficient for cellobiose utilization, while one of the transporters is required for utilization of the TCA cycle intermediate, citrate. Additionally, Cbr1 inhibits carbon catabolite repression, specifically during utilization of disaccharides, which may have evolved to limit the repression of genes encoding secreted proteins that cleave disaccharides into glucose extracellularly. The co-regulation of cellobiose and TCA cycle utilization with carbon catabolite repression may shed light on alternative methods of the regulation of carbon catabolite repression in fungi.

ORGANISM(S): Rhodotorula toruloides

PROVIDER: GSE293943 | GEO | 2025/04/10

REPOSITORIES: GEO

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Project description:Plant biomass holds tremendous potential as a renewable feedstock in the production of biofuels and biochemicals. The effective co-utilization of the main components cellulose and hemicellulose in plant lignocellulose is critical to the economic viability of lignocellulosic biorefineries. Here, we found that the thermophilic cellulolytic fungi Myceliophthora thermophila can utilize cellulose and hemicellulose synchronously. To investigate the underlying molecular mechanisms, we firstly checked the soluble carbohydrate of the culture using plant biomass (corncob) as sole carbon source and revealed the presence of various oligosaccharides including cellodextrin and xylodextrin, both intracellularly and extracellularly in the cultures, in addition to glucose or xylose. Based on these, intracellular oligosaccharide metabolism was proposed and confirmed by identification of cellodextrin and xylodextrin metabolism pathway. Furthermore, sugar consumption assay showed that contrasting with synchronous utilization of mixed cello-/xylo-dextrin, the inhibition effect of glucose for the metabolism of xylose and cello-/xylo-dextrin exists in this fungus, suggesting Carbon Catabolite Repression (CCR) is largely avoided at the form of oligosaccharides. Transporter MtCDT-2 showing preference to xylobiose and the tolerance of cellobiose inhibition also helps to bypass metabolic inhibition. Finally, the expression of cellulase and hemicellulase genes, were found orthogonal induction by cellobiose/Avicel and xylobiose/xylan, which conferred the ability of the strain to synchronously utilize cellulose and hemicellulose. Taken together, the orthogonal oligosaccharide catabolic pathway in this fungus establishes the molecular basis for the synchronous utilization of cellulose and hemicellulose, which sheds new light on understanding the plant biomass degradation by fungi and provides alternative paradigm for development of lignocellulose biorefinery such as consolidated bioprocessing in the future.

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Transcription factor reveals interconnected regulation of carbon source utilization and carbon catabolite repression in an oleaginous yeast

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