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 -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.