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Despite generally low primary productivity and diatom abundances in oligotrophic subtropical gyres, the North Atlantic Subtropical Gyre (NASG) exhibits significant diatom-driven carbon export on an annual basis. Subsurface pulses of nutrients likely fuel brief episodes of diatom growth, but the exact mechanisms utilized by diatoms in response to these nutrient injections remain understudied within near-natural settings. Here we simulated delivery of subsurface nutrients and compare the response among eukaryotic phytoplankton using a combination of physiological techniques and metatranscriptomics. We show that eukaryotic phytoplankton groups exhibit differing levels of transcriptional responsiveness and expression of orthologous genes in response to release from nutrient limitation. In particular, strategies for use of newly delivered nutrients are distinct among phytoplankton groups. Diatoms channel new nitrate to growth-related strategies while physiological measurements and gene expression patterns of other groups suggest alternative strategies. The gene expression patterns displayed here provide insights into the cellular mechanisms that underlie diatom subsistence during chronic nitrogen-depleted conditions and growth upon nutrient delivery that can enhance carbon export from the surface ocean.

Nitrogen availability limits marine productivity across large ocean regions. Diazotrophs can supply new nitrogen to the marine environment via nitrogen (N2) fixation, relieving nitrogen limitation. The distributions of diazotrophs and N2 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 N2 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, N2 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 N2 fixation rates. Overall, the occurrence of record-high UCYN-A abundance and peak N2 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 N2 fixation.

Nitrogen (N) is a limiting nutrient in vast regions of the world’s oceans, yet the sources of N available to various phytoplankton groups remain poorly understood. In this study, we investigated inorganic carbon (C) fixation rates and nitrate (NO3−), ammonium (NH4+) and urea uptake rates at the single cell level in photosynthetic pico-eukaryotes (PPE) and the cyanobacteria Prochlorococcus and Synechococcus. To that end, we used dual 15N and 13C-labeled incubation assays coupled to flow cytometry cell sorting and nanoSIMS analysis on samples collected in the North Pacific Subtropical Gyre (NPSG) and in the California Current System (CCS). Based on these analyses, we found that photosynthetic growth rates (based on C fixation) of PPE were higher in the CCS than in the NSPG, while the opposite was observed for Prochlorococcus. Reduced forms of N (NH4+ and urea) accounted for the majority of N acquisition for all the groups studied. NO3− represented a reduced fraction of total N uptake in all groups but was higher in PPE (17.4 ± 11.2% on average) than in Prochlorococcus and Synechococcus (4.5 ± 6.5 and 2.9 ± 2.1% on average, respectively). This may in part explain the contrasting biogeography of these picoplankton groups. Moreover, single cell analyses reveal that cell-to-cell heterogeneity within picoplankton groups was significantly greater for NO3− uptake than for C fixation and NH4+ uptake. We hypothesize that cellular heterogeneity in NO3− uptake within groups facilitates adaptation to the fluctuating availability of NO3− in the environment.

The ratio of dissolved oxygen to argon in seawater is frequently employed to estimate rates of net community production (NCP) in the oceanic mixed layer. The in situ O₂/Ar‐based method accounts for many physical factors that influence oxygen concentrations, permitting isolation of the biological oxygen signal produced by the balance of photosynthesis and respiration. However, this technique traditionally relies upon several assumptions when calculating the mixed‐layer O₂/Ar budget, most notably the absence of vertical fluxes of O₂/Ar and the principle that the air‐sea gas exchange of biological oxygen closely approximates net productivity rates. Employing a Lagrangian study design and leveraging data outputs from a regional physical oceanographic model, we conducted in situ measurements of O₂/Ar in the California Current Ecosystem in spring 2016 and summer 2017 to evaluate these assumptions within a “worst‐case” field environment. Quantifying vertical fluxes, incorporating nonsteady state changes in O₂/Ar, and comparing NCP estimates evaluated over several day versus longer timescales, we find differences in NCP metrics calculated over different time intervals to be considerable, also observing significant potential effects from vertical fluxes, particularly advection. Additionally, we observe strong diel variability in O₂/Ar and NCP rates at multiple stations. Our results reemphasize the importance of accounting for vertical fluxes when interpreting O₂/Ar‐derived NCP data and the potentially large effect of nonsteady state conditions on NCP evaluated over shorter timescales. In addition, diel cycles in surface O₂/Ar can also bias interpretation of NCP data based on local productivity and the time of day when measurements were made.

A multimethod process‐oriented investigation of diverse productivity measures in the California Current Ecosystem (CCE) Long‐Term Ecological Research study region, a complex physical environment, is presented. Seven multiday deployments covering a transition region from high to low productivity were conducted over two field expeditions (spring 2016 and summer 2017). Employing a Lagrangian study design, water parcels were followed over several days, comparing 24‐h in situ measurements (¹⁴C and¹⁵NO₃‐uptake, dilution estimates of phytoplankton growth, and microzooplankton grazing) with high‐resolution productivity measurements by fast repetition rate fluorometry (FRRF) and equilibrium inlet mass spectrometry (EIMS), and integrated carbon export measuremnts using sediment traps. Results show the importance of accounting for temporal and fine spatial scale variability when estimating ecosystem production. FRRF and EIMS measurements resolved diel patterns in gross primary and net community production. Diel productivity changes agreed well with comparably more traditional measurements. While differences in productivity metrics calculated over different time intervals were considerable, as those methods rely on different base assumptions, the data can be used to explain ecosystem processes which would otherwise have gone unnoticed. The processes resolved from this method comparison further understanding of temporal and spatial coupling and decoupling of surface productivity and potential carbon burial in a gradient from coastal to offshore ecosystems.