Distinct bacterial community structures with abundant carbon degradation and sulfur metabolisms found in different sea-ice types from the Central Arctic Ocean

The rapid decline of sea ice in the relatively understudied Central Arctic Ocean has a significant impact on bacterial biodiversity and the ecological functions they support. We investigated the bacterial community composition and the associated metabolic functions from three geographically distinct sea-ice floes: first-year ice (FYI) at the North Pole and western Nansen Basin and second-year or multi-year ice (SYI/MYI) in the western Amundsen Basin. We resolved the sea-ice bacterial community diversity at species-level precision using a long-read amplicon (<i>n</i> = 18) and metagenomic (<i>n</i> = 3) sequencing approach. The amplicon sequencing highlighted marked differences in bacterial community structure driven by ice age, floe origin, and environmental factors, demonstrating pronounced vertical structuring among ice horizons. Bacterial taxa like <i>Paraglaciecola psychrophila, Hydrogenophaga crassostreae, Octadecabacter arcticus, and Polaribacter irgensii</i> mainly dominated the bottom layers of SYI/MYI, whereas species <i>Actimicrobium antarcticum, Polaromonas cryoconiti, O. antarcticus,</i> and <i>Rhodoferax sp</i>. dominated the FYI. Similarly, notable taxonomic differences were observed in bacterial taxa inhabiting the surface and interior layers of FYI and SYI/MYI (e.g., <i>F. frigoris and Hydrogenophaga</i> sp.). The metagenomic analysis showed the prevalence of sulfur cycling-associated (assimilatory and dissimilatory sulfur metabolism) and complex carbon degradation processes in sea ice. We also elucidated the potential ecological role of novel metagenome-assembled genomes belonging to the genus <i>Aquiluna</i> through phylogenomic and pangenomic analyses. Overall, our findings revealed novel insights on the distinct bacterial communities that inhabit ice horizons and their associated ecological functions correlating with sea-ice type, origin, and habitat characteristics in the Central Arctic Ocean.IMPORTANCEThe Arctic region is warming nearly four times faster than the global average, leading to the continuous replacement of its thick multi-year sea ice with thinner first-year ice. The reduction in Arctic sea-ice cover was previously shown to have cascading effects on sea-ice-associated microbial communities and their role in the functioning of the ecosystem. This study provides the first high-resolution, species-level insight into the bacterial community composition and metabolic potential across different sea-ice types in the Central Arctic Ocean-an understudied yet rapidly changing environment. By combining long-read amplicon and metagenomic sequencing, we uncover distinct bacterial assemblages and functional metabolic roles that were shaped by the ice age and other physicochemical properties. Our findings highlight the ecological importance of sea-ice associated bacterial communities and the prevalence of sulfur metabolism and carbon degradation processes in different sea-ice types found in the central Arctic Ocean through genome-resolved metagenomics.