Microbial metabolism of complex organic matter across diverse deep-sea ecosystems

The deep sea is home to a vast and largely unexplored microbial biosphere, along with significant amounts of complex organic matter (COM). However, the ability of deep-sea microbes to metabolize complex organic matter across diverse regions remains poorly understood. Here, we combine 16S rRNA gene amplicon sequencing, metagenomics, and metatranscriptomics to comprehensively characterize prokaryotic communities across different years and habitats (cold seeps, hydrothermal vents, and seamounts). Our results reveal spatio-temporal community heterogeneity driven by geochemical gradients, alongside widespread genomic and transcriptomic potential for COM metabolism. Notably, the PVC (Planctomycetota-Verrucomicrobiota-Chlamydiota) superphylum exhibits extensive polysaccharide degradation capabilities, with Planctomycetota strain WC338 and Lentisphaerota strain WC36 isolated via laminarin enrichment. Growth and transcriptome data confirm their obligate laminarin dependence and robust degradation capacity, employing distinct enzymes (GH16 and GH2), whose broad distribution across diverse PVC superphylum lineages underscores their prevalence. Furthermore, we demonstrate that laminarin acts as a highly effective selective substrate for enriching and isolating the deep-sea PVC superphylum bacteria. Collectively, these findings delineate specialized adaptations within the PVC superphylum for polysaccharide degradation, significantly expanding our understanding of deep-sea microbial roles in global carbon cycling.