Assessment of the cellulolytic capacity of Streptomyces scabiei: evidence for regulatory constraints

Abstract

Streptomyces scabiei colonizes root and tuber crops and is the causative agent of common scab. It initiates its virulence through the perception of cello-oligosaccharides, particularly cellotriose, which signals living plant hosts, and cellobiose, which is more typical of decaying biomass. Given that both molecules derive from cellulose, this work investigated if and how S. scabiei has adapted its cellulolytic system to avoid unspecific activation of virulence in soil environments rich in plant-derived polysaccharides. Genomic analysis revealed that S. scabiei possesses a theoretically complete cellulolytic toolkit, including lytic polysaccharide monooxygenases, endoglucanases, and exoglucanases. However, despite this genetic potential, the bacterium exhibited only limited growth on insoluble cellulose, suggesting regulatory or translational constraints. Transcriptomic analyses confirmed strong induction of many cellulase genes by cellobiose and cellotriose, yet highlighted bottlenecks: most GH5 endoglucanases and the main LPMO gene (celS2) showed little or no induction, the later being also subjected to bldA-dependent translation control due to the presence of the rare TTA codon for leucine. Attempts to improve growth on cellulose by introducing a codon-optimized celS2 gene failed to enhance cellulose degradation or thaxtomin production, underscoring that synergistic enzyme activity are required. Supplementation experiments with exogenous cellobiose in cellulose-containing media revealed that only the highest concentrations improved growth, while thaxtomin production remained undetectable, suggesting diffusion and methodological limitations in solid media assays. Overall, this work demonstrates that S. scabiei has retained a full cellulolytic arsenal but tightly restricts its expression and activity, possibly as an adaptive strategy to ensure that virulence is triggered only in the presence of host-derived signals such as cellotriose. This regulatory tuning likely minimizes costly misactivation in soil environments rich in cellulose degradation products, thereby limiting the uptake of cellotriose only when in contact of its host. Future work using quantitative assays in liquid culture, microscopy, and metabolomic analyses will be essential to pinpoint the regulatory and enzymatic mechanisms that prevent cellulose utilization by S. scabiei.