Ecogenomic sensor reveals controls on N2-fixing microorganisms in the North Pacific Ocean

Abstract

Nitrogen-fixing microorganisms (diazotrophs) are keystone species that reduce atmospheric dinitrogen (N2) gas to fixed nitrogen (N), thereby accounting for much of N-based new production annually in the oligotrophic North Pacific. However, current approaches to study N2 fixation provide relatively limited spatiotemporal sampling resolution; hence, little is known about the ecological controls on these microorganisms or the scales over which they change. In the present study, we used a drifting robotic gene sensor to obtain high-resolution data on the distributions and abundances of N2-fixing populations over small spatiotemporal scales. The resulting measurements demonstrate that concentrations of N2 fixers can be highly variable, changing in abundance by nearly three orders of magnitude in less than 2 days and 30 km. Concurrent shipboard measurements and long-term time-series sampling uncovered a striking and previously unrecognized correlation between phosphate, which is undergoing long-term change in the region, and N2-fixing cyanobacterial abundances. These results underscore the value of high-resolution sampling and its applications for modeling the effects of global change.

Figure 1

BioLINCS environmental setting. (a) Sea-level anomaly (SLA: contours overlaid on all panels), sea surface temperature (SST) and near-surface chlorophyll concentrations are averages of satellite data from AVISO (Archiving, Validation and Interpretation of Satellite Oceanographic data) and MODIS (Moderate Resolution Imaging Spectroradiometer) Aqua, for 6–20 September 2011. The gray/black track shows the drift path of the instrumented platform (ESP, CTD and Acoustic Doppler Current Profiler (ADCP)), which began at the southernmost point. SLA image depicts eddies A and B, which influenced the ESP drift trajectory and are described in the text. The clockwise circulation of eddy A and associated stirring of regional water types is evident in the SST and chlorophyll patterns. Station ALOHA is marked by the circle+ symbol. (b) GOES (Geostationary Operational Environmental Satellites) SST from 12–13 September 2011 (nighttime). (c) Salinity along the ESP drift track, upper 80 m. (d) ESP drifter float (left) and base (right) are connected via an electromechanical cable. The ESP is sealed within the cylindrical pressure housing mounted to the platform base.

Figure 2

ESP drift contours of nutrient concentrations and ecological observations. (a) Platform velocity (speed in color, direction in track). Earth-referenced velocity of the ESP was determined from the time series of its GPS position. (b) Platform quasi-Lagrangian behavior based on the ESP-relative speed of water 3 m above the ESP. A water velocity of zero indicates Lagrangian movement (that is, perfect movement with the currents). (c) Salinity, with abundances of Atelocyanobacterium (in nifH gene copies per l). (d) Atelocyanobacterium are in red, Trichodesmium in orange and Crocosphaera in blue, plotted relative to the cruise transit distance. Solid lines indicate ESP-collected data and dotted lines are data from seawater collected from CTD niskins on board the ship. Diazotroph abundances are in agreement between the ESP and CTD. Chlorophyll, phosphate, nitrite and density are plotted versus depth and transit distance for this same period. Phosphate concentrations in surface waters are high but variable during the cruise. Relatively high nitrite concentrations extend from depth to the surface waters in the eastern portion of the inter-eddy transition zone, as the ESP circled twice due to contrasting currents. Numbers in red indicate ESP sample numbers (samples taken 16 h apart), corresponding with locations in Supplementary Figure 1. Stars indicate regions of lowest SLA sampled, where nutrients are highest in the surface waters. The red star in a and d also corresponds with the apex of the ESP transit.

Figure 3

Time series for the three most abundant diazotrophs during the present study and historical observations from Station ALOHA. (a) Atelocyanobacterium, Trichodesmium and Crocosphaera abundances over 3 to 6 years of monthly sampling at Station ALOHA (2008–2011). Summer months are darkened in gray. (b) Abundances of the same organisms during BioLINCS. See Supplementary Figure 3 for physical orientation by ESP sample number. Dotted lines delineate the range of abundances quantified during BioLINCS, demonstrating a heterogeneity in the Atelocyanobacterium and Trichodesmium populations that is comparable to the 3 years of summer patchiness data from ALOHA.

Figure 4

Regressions with phosphate. (a) The significant relationship between salinity and phosphate during the BioLINCS cruise allowed extrapolation of phosphate concentrations using salinity data, from ESP-collected samples. (b) Log of Atelocyanobacterium abundances versus phosphate concentrations. For remaining panels, squares correspond to BioLINCS eddy A samples, bold squares correspond with BioLINCS inter-eddy transition zone samples and dashed squares correspond with HOT data since 2008. The significant relationship between Atelocyanobacterium abundances and phosphate concentrations in the summer for all data sets since 2008 (note that here we show R²-values, whereas Pearson's correlation R-values are reported in the main text). (c) Positive relationship between the log of Crocosphaera abundances and phosphate concentrations (P=0.05). (d) Negative relationship between the log of Trichodesmium abundance versus phosphate concentration (P>0.05). Inset shows the same log of Trichodesmium abundances versus Crocosphaera abundances (R=−0.88; P<0.05); ‘X' designate the two outliers of this correlation. Abundances in the inter-eddy transition zone are elevated for the unicellular cyanobacteria, and depleted for Trichodesmium.