Symbiotic unicellular cyanobacteria fix nitrogen in the Arctic Ocean

Abstract

Biological dinitrogen (N₂) fixation is an important source of nitrogen (N) in low-latitude open oceans. The unusual N₂-fixing unicellular cyanobacteria (UCYN-A)/haptophyte symbiosis has been found in an increasing number of unexpected environments, including northern waters of the Danish Straight and Bering and Chukchi Seas. We used nanoscale secondary ion mass spectrometry (nanoSIMS) to measure ¹⁵N₂ uptake into UCYN-A/haptophyte symbiosis and found that UCYN-A strains identical to low-latitude strains are fixing N₂ in the Bering and Chukchi Seas, at rates comparable to subtropical waters. These results show definitively that cyanobacterial N₂ fixation is not constrained to subtropical waters, challenging paradigms and models of global N₂ fixation. The Arctic is particularly sensitive to climate change, and N₂ fixation may increase in Arctic waters under future climate scenarios.

Keywords: Arctic; cyanobacteria; marine microbiology; nanoSIMS; nitrogen fixation.

Fig. 1.

UCYN-A lineages are distributed throughout surface waters of the Western Arctic Ocean. Background colors represent sea-surface temperature on September 10, 2016 (www.esrl.noaa.gov). UCYN-A was quantified with qPCR. UCYN-A2 (black circles) is present at more stations, but UCYN-A1 (white circles) had the highest maximum abundance. Red stars indicate nanoSIMS measurement locations for ¹⁵N-uptake rates.

Fig. 2.

Arctic UCYN-A nifH sequences are identical to broadly distributed and abundant sequence types. Shown is a maximum likelihood phylogenetic tree of UCYN-A microdiversity based on partial nifH nucleotide sequences from a recent global survey (12). UCYN-A sequences from the Bering and Arctic Seas (red dots) are identical to dominant sequence types found in all major ocean basins. Regions where each sequence type has been found are specified by colored dots according to the legend; sequence counts from the global survey are also plotted. Nodes with bootstrap support >70 are identified with a diamond. Data from ref. .

Fig. 3.

Morphologies of Arctic UCYN-A symbioses are indistinguishable from subtropical strains. Double CARD-FISH comparison of UCYN-A lineages from the Bering Sea (A and C) and water collected at the Scripps Institute of Oceanography Pier in La Jolla, CA (B and D) show similar sizes and morphologies. CARD-FISH images show the symbiosis is intact, with both the haptophyte host (green and blue) and cyanobacteria (red). (Scale bar, 5 µm.)

Fig. 4.

UCYN-A symbioses fix ¹⁵N₂ in western Arctic waters. UCYN-A cell-specific ¹⁵N₂ fixation rates (A) and ¹⁵N enrichment (B–D) from nanoSIMS measurements after incubating natural populations in seawater with ¹⁵N₂. Bars of the same color (A) represent rates measured in individual symbioses (UCYN-A with host alga) from a single station and lineage (noted in underlying cell image). (Scale bar, 2 µm.) Averages are shown by a horizontal black line. Error bars are the SD of the cell-specific rate between the host and UCYN-A. Note the colored axes differ in scale on nanoSIMS images (B–D).