Abstract
Changing environmental conditions are of utmost importance for regulation of secondary metabolism in fungi. Different environmental cues including the carbon source, light and the presence of a mating partner can lead to altered production of compounds. Thereby, the heterotrimeric G-protein pathway is of major importance for sensing and adjustment of gene regulation. Regulation of secondary metabolism is crucial in the biotechnological workhorse Trichoderma reesei for knowledge-based adjustment in industrial fermentations, but also with respect to the potential use as a host for heterologous compound production. We investigated the function of the class VII G-protein coupled receptor (GPCR) gene gpr8 that is localized in the vicinity of the SOR cluster, which is responsible for biosynthesis of sorbicillinoids. GPR8 positively impacts regulation of the genes in this cluster in darkness. Accordingly, abundance of trichodimerol and dihydrotrichotetronine as well as other secondary metabolites is decreased in the deletion mutant. Transcriptome analysis moreover showed the major role of GPR8 being exerted in darkness with a considerable influence on regulation of secondary metabolism. Genes regulated in Δgpr8 overlap with those regulated directly or indirectly by the transcription factor YPR2, especially concerning genes related to secondary metabolism. The predicted FAD/FMN containing dehydrogenase gene sor7, one of the positive targets of the cascade triggered by GPR8, has a positive effect on secondary metabolite production, but also cellulase gene expression. Hence SOR7 has some overlapping, but also additional functions compared to GPR8. The G-protein coupled receptor GPR8 exerts a light dependent impact on secondary metabolism, which is in part mediated by the transcription factor YPR2 and the function of SOR7. Hence, T. reesei may apply GPR8 to adjust production of secondary metabolites and hence chemical communication to signals from the environment.
Highlights
TR_53238 is related to Aspergillus nidulans gprM (Lafon et al, 2006), which is involved in glucose sensing and sexual development (Dos Reis et al, 2019) and its N. crassa homolog NCU03253/gpr8 (Cabrera et al, 2015), that is indirectly regulated by the transcription factor ADV-1, which is necessary for transducing light signals and involved in controlling rhythms and cell fusion (Dekhang et al, 2017)
Among the genes up-regulated in gpr8 in darkness on cellulose we found significant enrichment of genes involved in secondary metabolism (p-value 1.36e-04), extracellular metabolism (p-value 3.10e-04) as well as extracellular protein degradation (p-value 1.53e-03) and interestingly on oxidative stress response (p-value 3.27e-03) and catalase reaction (p-value 6.34e-05)
We found that its function targets the SOR cluster, but influences secondary metabolism more broadly, likely targeting multiple regulators
Summary
Hypocrea jecorina) is one of the most prolific producers of plant cell wall degrading enzymes in industry. It has become a model organism for regulation of cellulase gene expression and plant cell wall degradation in general (Glass et al, 2013; Schmoll et al, 2016). Regulation of plant cell wall degrading enzymes is governed by a complex network of transcription factors and regulators (Benocci et al, 2017). Enzyme production is regulated by light in T. reesei on different carbon sources (Stappler et al, 2017a; Schmoll, 2018), resulting in strongly decreased cellulase levels in light compared to darkness (Stappler et al, 2017b)
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