New insights into the distributions of nitrogen fixation and diazotrophs revealed by high-resolution sensing and sampling methods

Abstract

Nitrogen availability limits marine productivity across large ocean regions. Diazotrophs can supply new nitrogen to the marine environment via nitrogen (N 2 ) fixation, relieving nitrogen limitation. The distributions of diazotrophs and N 2 fixation have been hypothesized to be generally controlled by temperature, phosphorus, and iron availability in the global ocean.However, even in the North Atlantic where most research on diazotrophs and N 2 fixation has taken place, environmental controls remain contentious. Here we measure diazotroph composition, abundance, and activity at high resolution using newly developed underway sampling and sensing techniques. We capture a diazotrophic community shift from Trichodesmium to UCYN-A between the oligotrophic, warm (25-29°C) Sargasso Sea and relatively nutrient-enriched, cold (13-24°C) subpolar and eastern American coastal waters. Meanwhile, N 2 fixation rates measured in this study are among the highest ever recorded globally and show significant increase with phosphorus availability across the transition from the Gulf Stream into subpolar and coastal waters despite colder temperatures and higher nitrate concentrations. Transcriptional patterns in both Trichodesmium and UCYN-A indicate phosphorus stress in the subtropical gyre. Over this iron-replete transect spanning the western North Atlantic, our results suggest that temperature is the major factor controlling the diazotrophic community structure while phosphorous drives N 2 fixation rates. Overall, the occurrence of record-high UCYN-A abundance and peak N 2 fixation rates in the cold coastal region where nitrate concentrations are highest (~200 nM) challenges current paradigms on what drives the distribution of diazotrophs and N 2 fixation.

High N2 Fixation in and Near the Gulf Stream Consistent with a Circulation Control on Diazotrophy

“…The N 2 fixation rates reported here are also between a factor of two and ten higher than nearby open ocean measurements: with rates between 6 and 18 nmol L −1 day −1 during this April cruise (Figure 1, Table S1), compared to rates consistently below 4 nmol L −1 day −1 measured in the open ocean subtropical North Atlantic gyre in August (Tang et al., 2019). These rates are consistent with those newly reported for the northwestern gyre (Tang et al., 2020).…”

Investigating the microbial ecology of coastal hotspots of marine nitrogen fixation in the western North Atlantic

“…The earlier discovery that UCYN-A is most likely responsible for observed coastal peaks in N 2 fixation in the Mid-Atlantic Bight and Southern New England Shelf 22 is intriguing given that UCYN-A is presumed to be an obligate endosymbiont of its host Braarudosphaera bigelowii . UCYN-A’s record abundances (up to 4 × 10 7 nifH copies L −1 ) 37 raise the question of what ecological conditions permit its host organism to be competitively successful and whether locally elevated N 2 fixation rates could be partially enabled by the success of the host phytoplankton in addition to the favorability of a niche for diazotrophic N 2 fixation.…”

“…Tang et al 2020 analyzed macronutrient and micronutrient concentrations within coastal ecosystems with high rates of N 2 fixation. They discovered these environments to be relatively replete in iron and nitrate, identifying phosphorus and temperature as key factors governing N 2 fixation activity and diazotrophic community structure, respectively 37 . In the same study, a nifH molecular survey identified UCYN-A as dominant in cold, subpolar coastal waters with diazotroph populations shifting towards Trichodesmium in warmer, oligotrophic waters offshore.…”

Bridging the Spatiotemporal Gap in Diazotroph Activity and Diversity With High-Resolution Measurements

“…Using an ecogenomic sensor, Robidart et al (2014) found that diazotroph abundances changed over three orders of magnitude in less than 2 days and 30 km in the North Pacific. Most recently, a microbiological autosampler collected 1 sample/h over a transect in the North Atlantic, showing record abundances of UCYN-A in cold coastal regions and less abundant Trichodesmium in warmer waters offshore (Tang et al, 2020). In the same region, another study with a spatial resolution of 1 sample each ∼5 km found peak abundances of Trichodesmium coinciding with steep gradients of current velocity at the edge of the Gulf Stream (Palter et al, 2020).…”

“…The acetylene reduction assay is based on the ability of the nitrogenase enzyme to reduce other triple-bonded molecules such as acetylene, which is reduced to ethylene and converted to N 2 fixation rates using a ratio of 3:1 or 4:1 depending on if hydrogen re-assimilation is considered or not (Stal, 1988;Capone, 1993), but just as with hydrogen measurements, empirically determined ratios vary widely (Mulholland et al, 2004(Mulholland et al, , 2006. Recently, this assay has been adapted to measure continuous N 2 fixation in underway seawater systems (Cassar et al, 2018;Tang et al, 2020). Indirect methods measure gross N 2 fixation rates, i.e., how much N 2 has been reduced by the nitrogenase enzyme, independent of whether it is channeled to diazotroph biomass or released extracellularly as dissolved nitrogen compounds.…”