The Polar Night Shift: Annual Dynamics and Drivers of Microbial Community Structure in the Arctic Ocean

Abstract

Change is a constant in the Arctic Ocean, with extreme seasonal differences in daylight, ice cover and temperature. The biodiversity and ecology of marine microbes across these extremes remain poorly understood. Here, using an array of autonomous samplers and sensors, we portray an annual cycle of microbial biodiversity, nutrient budgets and oceanography in the major biomes of the Fram Strait. In the ice-free West Spitsbergen Current, community turnover followed the solar cycle, with distinct separation of a productive summer state dominated by diatoms and carbohydrate-degrading bacteria, and a regenerative winter state dominated by heterotrophic Syndiniales, radiolarians, chemoautotrophic bacteria and archaea. Winter mixing of the water column replenishing nitrate, phosphate and silicate, and the onset of light were the major turning points. The summer succession of Phaeocystis, Grammonema and Thalassiosira coincided with ephemeral peaks of Formosa, Polaribacter and NS clades, indicating metabolic relationships between phytoplankton and bacteria. In the East Greenland Current, ice cover and greater sampling depth coincided with weaker seasonality, featuring weaker bloom/decay events and an ice-related winter microbiome. Low ice cover and advection of Atlantic Water coincided with diminished abundances of chemoautotrophic bacteria while Phaeocystis and Flavobacteriaceae increased, suggesting that Atlantification alters phytoplankton diversity and the biological carbon pump. Our findings promote the understanding of microbial seasonality in Arctic waters, illustrating the ecological importance of the polar night and providing an essential baseline of microbial dynamics in a region severely affected by climate change.

Seasonal bacterial niche structures and chemolithoautotrophic ecotypes in a North Atlantic fjord

“…These microbial recyclers play an important role in the global N-cycle, and in the Bedford Basin, winter mixing was identi ed as a major variable controlling the abundance and diversity of nitrifying organisms 31 . The seasonal changes in photoautotrophic production (with low alpha diversity) and heterotrophic recycling (with high alpha diversity) periods in our study complement the observations from the Arctic Ocean 37 . The interconnection between nutrient depletion and autotrophic biomass production in spring, and nutrient recycling and renewal in winter is a natural cycle which can be impacted by increasing ocean temperatures waters which prolong the strati cation of the mixed layer 52 .…”

“…Across the 4-year study, our results highlight a seasonal reversal in prokaryotic diversity in the upper water column relative to productivity and warmer waters in summer. These results complement the ndings of a peak in diversity in the temperate latitudes in winter at a regional scale in the English Channel 23 , in polar regions such as the Fram strait 37 and on a global scale 38 . The seasonal patterns which we observed in our data remained present at deeper rarefaction depths con rming the robustness of these trends (Supplementary Fig.…”

“…13), and ammoniaoxidizing species as indicator ASVs in winter months 31 . A similar seasonal succession from Flavobacteriain spring to nitrifying organisms in winter, has recently been shown in the Arctic and subarctic regions of the Atlantic Ocean 37 . Diminishing ice cover and the advection of warmer Atlantic water (referred to as atlanti cation) have been hypothesised to trigger a shift in phytoplankton diversity and a proportional increase in Flavobacteria at high latitudes.…”

“…Although global ocean surveys (e.g., TARA Oceans expeditions) have observed that highest prokaryotic diversity occurs near equatorial latitudes 32 , the lack of seasonal observations, compounded by the di culties of sampling during winter months in polar and temperate regions, bring into question our current perception of global microbial diversity patterns. Recent studies utilizing time series data have shown that species richness is negatively correlated with day length over an annual cycle with a highest richness peak in winter 23,37 . The nding that the relationship between temperature and diversity changes from a regional to a global scale reemphasises the need to adjust our sampling designs and analyses by seasons if we want to truly understand the drivers of marine prokaryotic richness and its in uence on the metabolic potential of the community 47 .…”

“…Diminishing ice cover and the advection of warmer Atlantic water (referred to as atlanti cation) have been hypothesised to trigger a shift in phytoplankton diversity and a proportional increase in Flavobacteria at high latitudes. Prolonged summer strati cation and reduced wintertime convection due to atlanti cation have been further shown to weaken deep-water renewal resulting in a decrease in associated "microbial recyclers", such as nitrifying Archaea and Bacteria in the Arctic 37 . These microbial recyclers play an important role in the global N-cycle, and in the Bedford Basin, winter mixing was identi ed as a major variable controlling the abundance and diversity of nitrifying organisms 31 .…”