Cellulose is an important component of particulate organic carbon in marine ecosystems and a critical component of the marine biological carbon pump. While microbial cellulose degradation in deep-sea sediment ecosystems has been documented, the specific cellulose-degrading potential and adaptive mechanisms of benthic piezophilic Alteromonas strains, as well as their specialized contributions to deep-sea carbohydrate cycling, remain poorly understood. Here we characterized Alteromonas sp. H39, a novel piezophilic bacterium isolated from deep-sea sediments, and investigated its cellulose-degrading capacity and adaptive evolution through integrated physiological, genomic, and comparative genomic approaches. Physiological assays indicated that this strain is a typical piezophile. Phylogenetically, strain H39 represents a putative novel species of Alteromonas, with ANI and dDDH values below the species delineation thresholds. Functional annotation identified 36 glycoside hydrolase families, including key cellulases. Growth assays confirmed its ability to utilize cellulose and a variety of other carbohydrates as sole carbon sources, with cellulase secretion verified through Congo red decolorization. Comparative genomic analysis of the genus Alteromonas revealed an open pan-genome structure, with strain H39 harboring a distinct repertoire of 666 strain-specific accessory genes. These unique genes showed significant enrichment in cold shock response, lipid metabolism, and nutrient transport, which are essential for adapting to extreme deep-sea environments. Notably, this strain is a pure culture experimentally validated piezophilic deep-sea Alteromonas bacterium with cellulolytic capacity. These findings highlight the distinct ecological role of piezophilic Alteromonas in deep-sea benthic carbon cycling and provide valuable genetic resources for marine cellulase biotechnology.
 

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