Transcriptomic insights into archaeal nitrification in the Amundsen Sea Polynya, Antarctica

Abstract

Abstract Background Ammonia-oxidizing archaea (AOA) are among the most ubiquitous and abundant microorganisms in the ocean, and play a primary role in the global nitrogen cycle. Antarctic polynyas are ecological hotspots with the highest primary productivity in the Southern Ocean during summer, and their production and formation reflect anthropogenic climate change. Strong seasonal variations in AOA abundance from winter to summer may have affected marine nitrification. We utilized metagenomics and metatranscriptomics to gain insights into the physiology and metabolism of AOA in polar oceans, which are associated with ecosystem functioning. Results A polar-specific ecotype of AOA, from the “Candidatus Nitrosomarinus”-like group, was observed to be dominant in the Amundsen Sea Polynya (ASP), West Antarctica, during a succession of summer phytoplankton blooms. AOA had the highest transcriptional activity among prokaryotes during the bloom decline phase (DC). Expression rank profiles for transcripts of key genes involved in ammonia oxidation (e.g., genes encoding subunits of ammonia monooxygenase, NirK, ferredoxin, and plastocyanin) and carbon fixation (3-hydroxypropionate/4-hydroxybutyrate cycle) indicated that AOA are actively involved in nitrification in the bloom DC. The highly ranked transcripts of flavodoxin and superoxide dismutase genes imply that AOA are exposed to iron limitation and ROS toxicity, respectively. The expression of high-affinity ammonia transporter (Amt2) gene, together with the absence of urea utilization-related genes, indicates that ammonia is a major source of AOA nitrification. The Phn system may aid AOA in acquiring phosphorus-containing compounds. The expression patterns of cdvA and cdvB also support the active cell division and cellular processes of AOA in the bloom DC. Conclusions The polar-specific ecotype AOA of “Candidatus Nitrosomarinus”-like group was found to be the representative AOA in the ASP, West Antarctica. Metatranscriptomic analysis of key genes involved in ammonia oxidation, carbon fixation, transport, and cell division indicated that this polar ecotype AOA was actively involved in nitrification in the bloom DC in the ASP. This study revealed the physiological and metabolic traits of this key polar-type AOA in response to phytoplankton blooms in the ASP and provided insights into AOA functions in polar oceans.