Deep long-read metagenomic sequencing reveals niche differentiation in carbon cycling potential between benthic and planktonic microbial populations

Coastal marine sediments function as large-scale natural biocatalytic filters, remineralizing and transforming organic matter. Benthic microbiomes exhibit remarkable temporal stability, contrasting with the dynamic, substrate-driven successions of bacterioplankton. Nonetheless, understanding their role in carbon cycling and interactions between these microbial groups is limited due to the complexity of benthic microbiomes. Here, we used a seasonally resolved, deep short- and long-read metagenomic approach to examine distinctive genomic features of microbiomes recovered from sediment, the overlaying water column, and particle-attached bacteria and archaea in the North Sea. We recovered 115 benthic metagenome-assembled genomes (MAGs) that belonged to Woeseiales , Rhizobiales , Planctomycetia , Gemmatimonadota , and Desulfobacterota species. While Proteobacteria and Actinobacteriota were characteristic phyla of sediments, Acidimicrobiia and Desulfocapsaceae species were shared between sediments and particle-attached fractions of the water column, indicative of significant bentho-pelagic coupling. Predominant members of the family Woeseiaceae carried polysaccharide utilization loci (PULs) predicted to target laminarin, alginate, and α-glucan in sediments. In contrast, water column species lacked PULs and encoded a significantly higher fraction of sulfatases and peptidases, indicating a role in the degradation of protein-rich and sulfated organic matter. Our findings disentangle family-level adaptations and niche differentiation between globally significant benthic and water column populations involved in marine organic matter degradation and carbon storage.