Abstract

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.

Highlights

  • Aquatic microorganisms drive global cycling of carbon, nitrogen, and many other elements by carrying out key ecosystem functions including primary production, organic matter remineralization, and transformations of inorganic compounds (Falkowski et al, 2008; Ferrera et al, 2015; Worden et al, 2015)

  • Alpha Diversity We identified 17,340 bacterial operational taxonomic units (OTUs) and 9,583 protistan OTUs

  • The presence of an increased relative abundance of chemoautotrophs suggests that iron, methane, nitrogen, and sulfur cycling are important under the ice during a time when the food web is often considered to be less productive

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Summary

Introduction

Aquatic microorganisms drive global cycling of carbon, nitrogen, and many other elements by carrying out key ecosystem functions including primary production, organic matter remineralization, and transformations of inorganic compounds (Falkowski et al, 2008; Ferrera et al, 2015; Worden et al, 2015). Climate change is warming the Arctic approximately two times faster than lower latitudes (Serreze and Barry, 2011), and is amplifying seasonal variations in temperature (Serreze and Barry, 2011), ice extent (Stroeve et al, 2012), and river flow (McClelland et al, 2006; Morison et al, 2012). Increased river runoff in spring is accelerating coastal ice melt (Whitefield et al, 2015), along the extensive Arctic continental shelf, where the interplay between these variables influences the timing and magnitude of biological production (Arrigo and van Dijken, 2015; Marchese et al, 2017), the species composition of primary producers (Li et al, 2009; Ardyna et al, 2014), and, in turn, higher and lower trophic levels (Wassmann et al, 2011; Vernet et al, 2017). Establishing the baseline relationship between microbial communities in Arctic coastal waters and their physical and chemical environment is key to understanding and predicting how they will respond to continued climate-induced changes to the Arctic system

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