Latitudinal patterns in ocean C:N:P reflect phytoplankton acclimation and macromolecular composition

Abstract

The proportions of carbon (C), nitrogen (N), and phosphorus (P) in surface ocean particulate matter deviate greatly from the canonical Redfield Ratio (C:N:P = 106:16:1) in space and time with significant implications for global carbon storage as this matter reaches the deep ocean. Recent work has revealed clear latitudinal patterns in C:N:P, yet the relative importance of ecological, physiological, or biochemical processes in creating these patterns is unclear. We present high-resolution, concurrent measurements of particulate C:N:P, macromolecular composition, environmental conditions, and plankton community composition from a transect spanning a subtropical-subpolar boundary, the North Pacific Transition Zone. We find that the summed contribution of macromolecules to particulate C, N, and P is consistent with, and provides interpretation for, particulate C:N:P patterns. A decline in particulate C:N from the subtropical to subpolar North Pacific largely reflects an increase in the relative contribution of protein compared to carbohydrate and lipid, whereas variation in C:P and N:P correspond to shifts in protein relative to polyphosphate, DNA, and RNA. Possible causes for the corresponding trends in C:N and macromolecular composition include physiological responses and changes in community structure of phytoplankton, which represented approximately 1/3^rd of particulate C across the transect. Comparison with culture experiments and an allocation-based model of phytoplankton macromolecular composition suggest that physiological acclimation to changing nutrient supply is the most likely explanation for the latitudinal trend in C:N, offering both a mechanistic interpretation and biochemical basis for large-scale patterns in C:N:P.

Keywords: acclimation; elemental stoichiometry; nutrients; phytoplankton.

Fig. 1.

(A) The mean sea surface temperature (SST) of the study area from 1955 to 2015 over the period of the cruise (27 May to 12 June), illustrating the environmental gradient spanning the North Pacific Subtropical Gyre (NPSG) and North Pacific TZ. Symbols on the map indicate major sampling points for the northbound (black) and southbound (white) portions of the cruise. Additional panels show the latitudinal variation in particulate carbon (B), particulate nitrogen (C), particulate phosphorus (D), dissolved inorganic nitrogen (DIN) (E), and community structure of phytoplankton ≤4 μm in estimated spherical diameter (F). The particulate element measurements represent 110 samples. The different symbols on panel E indicate samples collected by underway flow-through system at ~6 m depth (circle, n = 15) or by CTD-rosette at ~15 m depth (star, n = 15). Error bars in panel F indicate one SD among triplicate measurement at each discrete sample point (n = 15). The dashed line at 32.8°N delineates the subtropical gyre (NPSG) and TZ based on salinity while the dotted line at 36.2°N delineates the south transition zone (STZ) and north transition zone (NTZ) based on surface chlorophyll concentration (see Results and Discussion for regional boundary definitions).

Fig. 2.

Latitudinal variation in the macromolecular (n = 12) and total particulate (n = 110) molar ratio of (A) carbon:nitrogen, (B) carbon:phosphorus, and (C) nitrogen:phosphorus. Error bars for macromolecular ratios indicate one SD among replicate samples. The elemental contents of macromolecules in sampled particulate matter were calculated as described in Materials and Methods and in full detail in SI Appendix. The horizontal lines and inset of the vertical axis indicate the boundaries between the NPSG and the TZ (dashed line at 32.8°N) as well as the STZ and NTZ regions of the TZ (dotted line at 36.2°N). The vertical lines indicate the macromolecular elemental stoichiometry determined in N-starved cultures of Prochlorococcus marinus MED4 (cyan dotted lines), representative of the oligotrophic, picocyanobacteria-dominated NPSG, and nutrient-replete cultures of Ostreococcus tauri OTH95 (green dashed lines), representative of the more nutrient-rich, eukaryote-dominated NTZ.

Fig. 3.

The allocation (%) of macromolecular (A) carbon, (B) nitrogen, and (C) phosphorus among each macromolecular pool across the study area. Elemental contents of macromolecules were determined as described in the legend of Fig. 2 and SI Appendix. The error among replicate samples is not shown but was generally low (mean of 12% variation) and is shown in SI Appendix, Tables S6–S8. The arrow at the bottom of the figure indicates the decreasing nutrient supply and increasing N-limitation moving southward from the NTZ to the NPSG. The vertical lines and inset of the horizontal axis indicate regional boundaries.

Fig. 4.

The predicted growth rate (A), macromolecular C:N (B), and proportion (%) of macromolecular C found in (C) protein as well as the (D) the sum of carbohydrate and lipid for phytoplankton size classes of 0.5, 1.0, and 3.0 µm equivalent spherical diameter (solid and dashed lines). Observed values of macromolecular elemental stoichiometry and contribution to macromolecular C are shown as discrete symbols in panels B–D for comparison (n = 12). Error bars indicate one SD among duplicate (%C in Carb. and Lipid) or triplicate (%C in Protein) samples. The vertical lines and inset of the horizontal axis indicate regional boundaries.