Nitrogen cycling during an Arctic bloom: from chemolithotrophy to nitrogen assimilation.

Abstract

In the Arctic, phytoplankton blooms are recurring phenomena occurring during the spring-summer seasons and influenced by the strong polar seasonality. Bloom dynamics are affected by nutrient availability, especially nitrogen, which is the main limiting nutrient in the Arctic. This study aimed to investigate the changes in an Arctic microbial community using omics approaches during a phytoplankton bloom focusing on the nitrogen cycle. Using metagenomic and metatranscriptomic samples from the Dease Strait (Canada) from March to July (2014), we reconstructed 176 metagenome-assembled genomes. Bacteria dominated the microbial community, although archaea reached up to 25% of metagenomic abundance in early spring, when Nitrososphaeria archaea actively expressed genes associated with ammonia oxidation to nitrite (amt, amo, nirK). The resulting nitrite was presumably further oxidized to nitrate by a Nitrospinota bacterium that highly expressed a nitrite oxidoreductase gene (nxr). Since May, the constant increase in chlorophyll a indicated the occurrence of a phytoplankton bloom, promoting the successive proliferation of different groups of chemoorganotrophic bacteria (Bacteroidota, Alphaproteobacteria, Gammaproteobacteria). These bacteria showed different strategies to obtain nitrogen, whether it be from organic or inorganic sources, according to the expression patterns of genes encoding transporters for nitrogen compounds. In contrast, during summer, the chemolithotrophic organisms thriving during winter reduced their relative abundance and the expression of their catabolic genes. Based on our functional analysis, we see a transition from a community where nitrogen-based chemolitotrophy plays a relevant role to a chemoorganotrophic community based on the carbohydrates released during the phytoplankton bloom, where different groups seem to specialize in different nitrogen sources.IMPORTANCEThe Arctic is one of the environments most affected by anthropogenic climate change. It is expected that the rise in temperature and change in ice cover will impact the marine microbial communities and the associated biogeochemical cycles. In this regard, nitrogen is the main nutrient limiting Arctic phytoplankton blooms. In this study, we combine genetic and expression data to study the nitrogen cycle at the community level over a time series covering from March to July. Our results indicate the importance of different taxa (from archaea to bacteria) and processes (from chemolithoautotrophy to incorporation of different nitrogen sources) in the cycling of nitrogen during this period. This study provides a baseline for future research that should include additional methodologies like biogeochemical analysis to fully understand the changes occurring on these communities due to global change.