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. Besides, bloom dynamics is 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 during a phytoplankton bloom with a special focus 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 genomic abundance in early spring, when Nitrososphaeria archaea actively expressed genes associated with ammonia oxidation to nitrite (amt, amoA, 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 (Bacteroidetes, Alphaproteobacteria and Gammaproteobacteria). These bacterial taxa 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 the functional analysis of our data, 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 specialize in different nitrogen sources.