Genomic architecture and transcriptional regulation of cellulose degradation in the novel marine bacterium Pseudoxanthomonas sp. JC1303.

Microbial degradation of cellulose is a fundamental process driving the global carbon cycle and holds immense potential for sustainable biotechnology; however, the genomic mechanisms and transcriptional regulation underlying this capability in marine environments remain largely underexplored. To decipher these complex biological strategies, we isolated the novel strain JC1303 from marine sediments and integrated whole-genome sequencing with transcriptomic analysis to systematically characterize its enzymatic arsenal and metabolic adaptations. Whole-genome sequencing revealed that strain JC1303 possesses a circular chromosome of 4.37 Mb in length, with a GC content of 67.41%. Phylogenetic analyses based on the 16 S rRNA gene and whole-genome data suggest that strain JC1303 likely represents a new species within the genus Pseudoxanthomonas. Pan-genome analysis of the genus demonstrates a typical "open" genome architecture with only 3% conserved core genes, highlighting high evolutionary plasticity. In contrast, strain JC1303 has 936 unique genes significantly enriched in metabolism (163 genes) and signal transduction (138 genes), providing a molecular basis for its adaptation to the cellulose degradation niche. Genome mining identified a complete cellulolytic system comprising three endo-β-1,4-glucanases, two cellulase, and four β-1,4-glucosidase, supported by glycolysis/gluconeogenesis, TCA cycle, pentose phosphate pathway, amino acid synthesis pathways, ABC transport systems, and the respiratory chain. Crucially, comparative transcriptomic profiling under cellulose induction validated the functional execution of this genetic potential. Among 1465 differentially expressed genes, the strain exhibited a coordinated strategy: while distinct isozymes were downregulated, a key endoglucanase gene (JC1303_01352) and multiple membrane transporter genes were significantly upregulated. This suggests a specific mechanism coupling extracellular hydrolysis with efficient substrate uptake. In conclusion, this study not only elucidates the genetic blueprint and transcriptional regulation of a new marine cellulolytic species Pseudoxanthomonas JC1303 but also offers theoretical support for engineering robust biocatalysts.