Nitrate Assimilation by Eukaryotic Phytoplankton as a Central Characteristic of Ocean Productivity

Abstract

Biologically available nitrogen (N) is essential for phytoplankton growth, such that N availability can limit marine productivity and determine phytoplankton community composition. N is supplied to the upper ocean either as (1) "new" N, nitrate mixed up from the ocean interior, augmented by N2 fixation, or (2) "recycled" N, ammonium and simple organic forms regenerated in surface waters. Annually, production fueled by new N is balanced by the sinking of organic matter out of surface waters, maintaining the sequestration in the ocean interior of atmospheric CO2 fixed as biomass (the "biological pump"). The contributions of different phytoplankton groups to total production and carbon export are poorly constrained. Identifying the N sources that support these phytoplankton groups, and understanding their dynamics and physical controls, will greatly improve those constraints.

The most productive oceanic regions are associated with eastern boundary currents where the upwelling of cold, nutrient-replete waters stimulates phytoplankton blooms. Diatoms typically constitute the majority of large phytoplankton in these systems, although the exact mechanism for diatom success has never been explicitly demonstrated. To investigate differential phytoplankton N use during upwelling, an upwelling event - and subsequent phytoplankton bloom - was simulated in a mesocosm experiment beginning with Monterey Bay subsurface water. This dissertation presents the first direct evidence that the mechanism by which diatoms come to dominate high nitrate environments is an early acceleration, and subsequent maintenance, of their specific nitrate uptake rate. This strategy allows diatoms to grow quickly and consume a disproportionate fraction of the available nutrients.

In contrast to upwelling regions, the subtropical ocean is characterized by intense surface stratification that limits the nitrate supply from below such that regenerated N is assumed to fuel most phytoplankton growth. This dissertation describes a new approach for characterizing the N sources to taxonomically distinct components of particulate N (PN) suspended in surface waters: coupling flow cytometry with a highly sensitive method for N isotope analysis of particles (PN) collected from the Sargasso Sea euphotic zone in March, July, October, and December.

Throughout the year, the low <super>15</super>N/<super>14</super>N of <italic>Prochlorococcus</italic> indicates reliance on recycled N. <italic>Synechoccocus</italic> <super>15</super>N/<super>14</super>N also evinces recycled N consumption in the summer and fall, whereas in March, <italic>Synechoccocus</italic> <super>15</super>N/<super>14</super>N was more variable and higher than <italic>Prochlorococcus</italic>, implying that <italic>Synechoccocus</italic> assimilates nitrate during springtime conditions of high availability.

In July, the <super>15</super>N/<super>14</super>N of the less abundant eukaryotic phytoplankton was consistently higher than that of the prokaryotes, reflecting consumption of subsurface nitrate, despite its vanishingly low concentration in surface waters. This high eukaryote <super>15</super>N/<super>14</super>N implies that sinking material derives largely from eukaryotic, not prokaryotic, phytoplankton biomass, suggesting that the eukaryotic contribution to carbon sequestration in the ocean interior is substantially greater than their contribution to total net primary production; thus, the biological pump in the subtropical ocean appears to be driven mostly by eukaryotic phytoplankton.

In October and December, two eukaryote profiles yielded the same findings as in July, while in three other profiles, eukaryote <super>15</super>N/<super>14</super>N was similar to that of the prokaryotes, suggesting a switch toward more complete reliance on recycled N. This change in N preference appears to be driven by the density structure of the upper water column. In July, the very shallow low-density surface "mixed layer" does not contribute to stratification at the base of the euphotic zone, and subsurface nitrate can mix up into the photosynthetically-active layer. Mixed layer deepening into the fall, typically taken as an indication of weaker overall stratification, actually strengthens the density-driven isolation of the euphotic zone, reducing the upward supply of nitrate. In the spring, vertical mixing erodes surface stratification, entraining nitrate into the euphotic zone that was consumed with an isotope effect by eukaryotes. Annually, therefore, eukaryotic phytoplankton dominate both new and export production in the Sargasso Sea.

The research described in this dissertation was conducted in highly contrasting regions of the ocean, yet a common finding has emerged: larger and/or more physiologically complex phytoplankton (eukaryotes in general and diatoms in upwelling regimes) specialize in the acquisition of nitrate supplied from the ocean interior. Interestingly, these phytoplankton are also more readily removed to the deep ocean where their biomass is remineralized to nitrate. The dominant N source assimilated by eukaryotic phytoplankton is thus biased towards the form of N resulting from the remineralization of their own biomass. This raises the possibility that the evolution of N uptake strategy by eukaryotic phytoplankton has been partially guided by the fate of eukaryotic biomass.