The arabinose transporter MtLat-1 is involved in hemicellulase repression as a pentose transceptor in Myceliophthora thermophila

Abstract

Background Filamentous fungi possess an array of secreted enzymes to depolymerize the structural polysaccharide components of plant biomass. Sugar transporters play an essential role in nutrient uptake and sensing of extracellular signal molecules to inhibit or trigger the induction of lignocellulolytic enzymes. However, the identities and functions of transceptors associated with the induction of hemicellulase genes remain elusive. Results In this study, we reveal that the l-arabinose transporter MtLat-1 is associated with repression of hemicellulase gene expression in the filamentous fungus Myceliophthora thermophila. The absence of Mtlat-1 caused a decrease in l-arabinose uptake and consumption rates. However, mycelium growth, protein production, and hemicellulolytic activities were markedly increased in a ΔMtlat-1 mutant compared with the wild-type (WT) when grown on arabinan. Comparative transcriptomic analysis showed a different expression profile in the ΔMtlat-1 strain from that in the WT in response to arabinan, and demonstrated that MtLat-1 was involved in the repression of the main hemicellulase-encoding genes. A point mutation that abolished the l-arabinose transport activity of MtLat-1 did not impact the repression of hemicellulase gene expression when the mutant protein was expressed in the ΔMtlat-1 strain. Thus, the involvement of MtLat-1 in the expression of hemicellulase genes is independent of its transport activity. The data suggested that MtLat-1 is a transceptor that senses and transduces the molecular signal, resulting in downstream repression of hemicellulolytic gene expression. MtAra-1 protein directly regulated the expression of Mtlat-1 by binding to its promoter region. Transcriptomic profiling indicated that the transcription factor MtAra-1 also plays an important role in expression of arabinanolytic enzyme genes and l-arabinose catabolism. Conclusions M. thermophila MtLat-1 functions as a transceptor that is involved in l-arabinose transport and signal transduction associated with suppression of the expression of hemicellulolytic enzyme-encoding genes. The data presented in this study add to the models of the regulation of hemicellulases in filamentous fungi.

Correlating sugar transporter expression and activities to identify transporters for an orphan sugar substrate

“…The diversity of transporters involved in membrane trafficking of sugars has likely evolved from the single function of glucose uptake into the cells (Carbó and Rodríguez 2023 ). In addition to their great biological importance in cell nutrition and homeostasis, sugar transporters can act as “transceptors” with essential functions for sensing, not only of glucose but also for other sugars such as l -arabinose and cellobiose (Celenza et al 1988 ; Madi et al 1997 ; Kim et al 2013 ; Znameroski et al 2014 ; Gu et al 2023 ). By their involvement in sugar perception, sugar transporters trigger signaling cascades, leading to the induction of biomass-hydrolyzing enzymes such as cellulases and hemicellulases (Adnan et al 2017 ; Wu et al 2020 ; Mattam et al 2022 ).…”