Abstract
BackgroundThe glucose dual-affinity transport system (low- and high-affinity) is a conserved strategy used by microorganisms to cope with natural fluctuations in nutrient availability in the environment. The glucose-sensing and uptake processes are believed to be tightly associated with cellulase expression regulation in cellulolytic fungi. However, both the identities and functions of the major molecular components of this evolutionarily conserved system in filamentous fungi remain elusive. Here, we systematically identified and characterized the components of the glucose dual-affinity transport system in the model fungus Neurospora crassa.ResultsUsing RNA sequencing coupled with functional transport analyses, we assigned GLT-1 (Km = 18.42 ± 3.38 mM) and HGT-1/-2 (Km = 16.13 ± 0.95 and 98.97 ± 22.02 µM) to the low- and high-affinity glucose transport systems, respectively. The high-affinity transporters hgt-1/-2 complemented a moderate growth defect under high glucose when glt-1 was deleted. Simultaneous deletion of hgt-1/-2 led to extensive derepression of genes for plant cell wall deconstruction in cells grown on cellulose. The suppression by HGT-1/-2 was connected to both carbon catabolite repression (CCR) and the cyclic adenosine monophosphate-protein kinase A pathway. Alteration of a residue conserved across taxa in hexose transporters resulted in a loss of glucose-transporting function, whereas CCR signal transduction was retained, indicating dual functions for HGT-1/-2 as “transceptors.”ConclusionsIn this study, GLT-1 and HGT-1/-2 were identified as the key components of the glucose dual-affinity transport system, which plays diverse roles in glucose transport and carbon metabolism. Given the wide conservation of the glucose dual-affinity transport system across fungal species, the identification of its components and their pleiotropic roles in this study shed important new light on the molecular basis of nutrient transport, signaling, and plant cell wall degradation in fungi.
Highlights
The glucose dual-affinity transport system is a conserved strategy used by microorganisms to cope with natural fluctuations in nutrient availability in the environment
Glucose sensing and uptake are critical for cellulase expression regulation via carbon catabolite repression (CCR) [4, 5]; elucidating the molecular basis of glucose transport is critical for plant biomass deconstruction and bio-based chemical and fuel production
To obtain a broad view of the mode of expression and to define the functional molecular elements of the dual-affinity transport system, we conducted high-throughput sequencing (RNA-Seq) of wild-type (FGSC2489) mycelia exposed to a gradient of glucose (0, 0.05, 0.5, 2.0, 10.0%) for 1 or 2 h
Summary
The glucose dual-affinity transport system (low- and high-affinity) is a conserved strategy used by microorganisms to cope with natural fluctuations in nutrient availability in the environment. The glucose-sensing and uptake processes are believed to be tightly associated with cellulase expression regulation in cellulolytic fungi. Both the identities and functions of the major molecular components of this evolutionarily conserved system in filamentous fungi remain elusive. Glucose sensing and uptake are critical for cellulase expression regulation via carbon catabolite repression (CCR) [4, 5]; elucidating the molecular basis of glucose transport is critical for plant biomass deconstruction and bio-based chemical and fuel production. The genes of this dual system have still not been uncovered and their functions remain to be dissected
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