Characteristics of deep-sea microbial cellulases: key determinants of the ultimate fate of plant biomass on Earth

Abstract

Land plants, especially those with significant woody biomass, represent the largest source of biomass on Earth, making the biodegradation of lignocellulosic materials critical to understanding the global carbon cycle. Cellulose, a major component of lignocellulose, is notoriously resistant to degradation due to its highly crystalline structure. While the degradation of cellulose by terrestrial microbes has been extensively studied, the mechanisms of cellulose degradation in deep-sea environments remain largely unexplored. The deep-sea ecosystem depends on organic matter, such as cellulose, that is synthesized in terrestrial environments and surface waters and descends to the deep sea. Recent studies suggest that a significant amount of cellulose is likely to reach the deep sea. Here, we present an in-depth study of cellulases from a novel deep-sea γ-proteobacterial strain TOYAMA8, isolated from Toyama Bay, Japan, using Surface Pitting Observation Technology (SPOT), a highly sensitive assay for enzymatic cellulose hydrolysis. The cellulases of strain TOYAMA8 show similarities to those of a previously reported deep-sea cellulolytic microbe, Marinagarivorans cellulosilyticus strain GE09. Genomic and transcriptomic analyses of these strains reveal novel cellulase genes and mechanisms that differ from terrestrial counterparts, shedding light on the unique adaptations of deep-sea microbes to recalcitrant biomass. In particular, these strains produce high-molecular-weight cellulases with unique domain architectures, likely optimized for membrane anchoring, which prevents enzyme diffusion and ensures efficient localized activity. Our findings provide critical insights into the microbial cellulose degradation in the deep sea, highlighting its role in the fate of organic carbon and the potential for biotechnological applications in biorefineries.