Strong Seasonality in Arctic Estuarine Microbial Food Webs

Microbial communities in the coastal Arctic Ocean experience extreme variability in organic matter and inorganic nutrients driven by seasonal shifts in sea ice extent and freshwater inputs. Lagoons border more than half of the Beaufort Sea coast and provide important habitats for migratory fish and seabirds; yet, little is known about the planktonic food webs supporting these higher trophic levels. To investigate seasonal changes in bacterial and protistan planktonic communities, amplicon sequences of 16S and 18S rRNA genes were generated from samples collected during periods of ice-cover (April), ice break-up (June), and open water (August) from shallow lagoons along the eastern Alaska Beaufort Sea coast from 2011 through 2013. Protist communities shifted from heterotrophic to photosynthetic taxa (mainly diatoms) during the winter-spring transition, and then back to a heterotroph-dominated summer community that included dinoflagellates and mixotrophic picophytoplankton such as Micromonas and Bathycoccus. Planktonic parasites belonging to Syndiniales were abundant under ice in winter at a time when allochthonous carbon inputs were low. Bacterial communities shifted from coastal marine taxa (Oceanospirillaceae, Alteromonadales) to estuarine taxa (Polaromonas, Bacteroidetes) during the winter-spring transition, and then to oligotrophic marine taxa (SAR86, SAR92) in summer. Chemolithoautotrophic taxa were abundant under ice, including iron-oxidizing Zetaproteobacteria. These results suggest that wintertime Arctic bacterial communities capitalize on the unique biogeochemical gradients that develop below ice near shore, potentially using chemoautotrophic metabolisms at a time when carbon inputs to the system are low. Co-occurrence networks constructed for each season showed that under-ice networks were dominated by relationships between parasitic protists and other microbial taxa, while spring networks were by far the largest and dominated by bacteria-bacteria co-occurrences. Summer networks were the smallest and least connected, suggesting a more detritus-based food web less reliant on interactions among microbial taxa. Eukaryotic and bacterial community compositions were significantly related to trends in concentrations of stable isotopes of particulate organic carbon and nitrogen, among other physiochemical variables such as dissolved oxygen, salinity, and temperature. This suggests the importance of sea ice cover and terrestrial carbon subsidies in contributing to seasonal trends in microbial communities in the coastal Beaufort Sea.