Transpolar Drift and Atlantic inflow shape microbial biogeography and metabolic processes across the central Arctic Ocean

The Arctic Ocean is changing rapidly. Sea-ice loss, advancing Atlantification and terrigenous inputs create contrasting ecoregions, yet their underlying microbial processes remain unresolved. Here, we combine high-resolution oceanographic observations and multi-omics data from the North Pole to the Svalbard shelf to determine how the shift from terrigenous influence to Atlantic-dominated waters shapes microbial biogeography, community assembly and metabolic processes. We demonstrate distinct, lifestyle-specific differences in microbial communities across four hydrographic regimes, with particle-attached communities showing a predominantly stochastic distribution while free-living communities were more regime-dependent. In the terrigenous-influenced Amundsen Basin, particle-attached microbial communities drive degradation of recalcitrant terrigenous organic matter with enrichment in denitrification, suggesting potential net nitrogen loss. Moving into Atlantic-dominated waters in the Nansen Basin during late summer, free-living communities increasingly rely on mixotrophic scavenging, trace gas oxidation and marine organic matter cycling as waters become progressively more nutrient-depleted. Surface-driven photoheterotrophy prevails in the warmest, ice-free waters. Comparative genomics across the Arctic Ocean further demonstrates highly connected yet regionally adapted microbial communities governed by these distinct hydrographic regimes. These results offer a mechanistic view of how microbial metabolic processes may restructure as the region becomes seasonally ice-free, Atlantification intensifies, and terrigenous inputs increase, thereby reshaping biogeochemical cycling across the Arctic Ocean.