The polar night shift: seasonal dynamics and drivers of Arctic Ocean microbiomes revealed by autonomous sampling

The Arctic Ocean features extreme seasonal differences in daylight, temperature, ice cover, and mixed layer depth. However, the diversity and ecology of microbes across these contrasting environmental conditions remain enigmatic. Here, using autonomous samplers and sensors deployed at two mooring sites, we portray an annual cycle of microbial diversity, nutrient concentrations and physical oceanography in the major hydrographic regimes of the Fram Strait. The ice-free West Spitsbergen Current displayed a marked separation into a productive summer (dominated by diatoms and carbohydrate-degrading bacteria) and regenerative winter state (dominated by heterotrophic Syndiniales, radiolarians, chemoautotrophic bacteria, and archaea). The autumn post-bloom with maximal nutrient depletion featured Coscinodiscophyceae, Rhodobacteraceae (e.g. Amylibacter) and the SAR116 clade. Winter replenishment of nitrate, silicate and phosphate, linked to vertical mixing and a unique microbiome that included Magnetospiraceae and Dadabacteriales, fueled the following phytoplankton bloom. The spring-summer succession of Phaeocystis, Grammonema and Thalassiosira coincided with ephemeral peaks of Aurantivirga, Formosa, Polaribacter and NS lineages, indicating metabolic relationships. In the East Greenland Current, deeper sampling depth, ice cover and polar water masses concurred with weaker seasonality and a stronger heterotrophic signature. The ice-related winter microbiome comprised Bacillaria, Naviculales, Polarella, Chrysophyceae and Flavobacterium ASVs. Low ice cover and advection of Atlantic Water coincided with diminished abundances of chemoautotrophic bacteria while others such as Phaeocystis increased, suggesting that Atlantification alters microbiome structure and eventually the biological carbon pump. These insights promote the understanding of microbial seasonality and polar night ecology in the Arctic Ocean, a region severely affected by climate change.