Upward nitrate transport by phytoplankton in oceanic waters: balancing nutrient budgets in oligotrophic seas

Abstract

In oceanic gyres, primary producers are numerically dominated by small (1-5 µm diameter) pro-and eukaryotic cells that primarily utilize recycled nutrients produced by rapid grazing turnover in a highly efficient microbial loop. Continuous losses of nitrogen to depth by sinking, either as single cells, aggregates or fecal pellets, are balanced by both nitrate inputs at the base of the euphotic zone and nitrogen-fixation. This input of N (new nitrogen) to balance export losses (the biological pump) is a fundamental aspect of nitrogen cycling and central to understanding carbon fluxes in the ocean. In the Pacific Ocean, detailed nitrogen budgets at the time-series station HOT require upward transport of nitrate from the nutricline (80-100 m) into the surface layer (~0-40 m) to balance productivity and export needs. However, concentration gradients are negligible and cannot support the fluxes. Physical processes can inject nitrate into the base of the euphotic zone, but the mechanisms for transporting this nitrate into the surface layer across many 10s of m in highly stratified systems are unknown.In these seas, vertical migration by the very largest 10 2 -10 3 µm diameter) phytoplankton is common as a survival strategy to obtain nitrogen from sub-euphotic zone depths. This vertical migration is driven by buoyancy changes rather than by flagellated movement and can provide upward nitrogen transport as nitrate (mM concentrations) in the cells. However, the contribution of vertical migration to nitrate transport has been difficult to quantify over the required basin scales. In this study, we use towed optical systems and isotopic tracers to PrePrintsIntroduction Nitrogen in the euphotic zone of the open sea has long been recognized to partition into two distinct pools of availability (Dugdale & Goering 1967). New nitrogen represents introduction of N from outside the euphotic zone, either in the form of deep NO 3 -or nitrogenfixation, while regenerated N results from consumption and remineralization of dissolved or particulate N (Dugdale & Goering 1967). While regenerated N dominates the total phytoplankton uptake, new N is critical to balance losses due to vertical fluxes and is linked to total system productivity (Eppley & Peterson 1979). This has been expressed as the f ratio where 'f' = new/total N uptake and ranges from 0-1. On longer time scales, new N input must balance sedimentary losses or the system will experience net losses of nitrogen (Eppley & Peterson 1979). The surface waters of the open ocean are considered low 'f' ratio environments: N and P often occur at nM concentrations, and ammonium is the dominant form taken up by phytoplankton (Lipschultz et al. 1996;Raimbault et al. 2008;Wu et al. 2000). The f ratio increases in the light-limited lower depths of the euphotic zone due to the increased availability of nitrate at the nutricline, thus creating what has been recognized as a two-layered structure (Goldman 1988). This general pattern can be modified in regions of low iron input, where iron ava...

Periodic and coordinated gene expression between a diazotroph and its diatom host

“…Currently, only a few genera of diatoms are known to form symbiotic relationships with diazotrophs. Further, Rhizosolenia is known to exist without Richelia [10] suggesting this partnership is facultative. Although the transfer of N from symbionts to diatom hosts has been demonstrated [6,11], there are no long-term cultures of this symbiosis to study and our current understanding of this association in situ is limited.…”

Vertically migrating phytoplankton drive seasonal formation of subsurface negative preformed nitrate anomalies in the subtropical North Pacific and North Atlantic

“…Flagellate motility and cyanobacteria buoyancy control has been recognized for decades as a strategy to exploit spatially disjunct light and nutrient fields (Cullen, 1985;Eppley et al, 1968, Ganf andOliver, 1982;Hasle, 1950;Steemann Nielsen, 1939) and was first suggested for non-flagellated marine species in Pyrocystis (Ballek and Swift, 1986;Rivkin et al, 1984). Fraga et al (1992Fraga et al ( , 1999 (Villareal et al, 1993, Villareal et al, 2014, internal millimolar nitrate pools that can only be acquired by direct uptake at µM concentrations (Villareal and Lipschultz, 1995;Villareal et al, 1996;Woods and Villareal, 2008), buoyancy reversals linked to nutrient status (Richardson et al, 1996), nitrate reductase activity (Joseph et al, 1997) induced only when nitrate is the primary N source, ascent/descent rates of m hr -1 (Villareal et al, 2014;Moore and Villareal 1996), observation of Rhizosolenia mats from the surface to 305 m (Pilskaln et al, 2005), and compositional difference in floating and sinking mats that mirror physiological changes associated with nutrient depletion and carbohydrate ballasting (Villareal et al, 1996). The m hr -1 ascent/descent rates permit the necessary 50-100 m vertical excursions and when coupled with the large vacuole of these giant phytoplankton, allow the necessary storage (mM concentrations in vacuoles that are 90+% of total cell volume) for a multiple day migration and division cycle.…”

“…Giant phytoplankton are found throughout the warmer oceans of the world and the required characteristics of buoyancy reversals, high internal nitrate pools and rapid ascent have been found in multiple taxa from the Atlantic and Pacific Oceans (Villareal et al, 2014). Unlike the more widely known zooplankton vertical migration, open ocean phytoplankton migration is a multi-day cycle (Richardson et al, 1998;Villareal et al, 1996).…”

Active water transport in unicellular algae: where, why, and how

“…However, active water transport may also be a mechanism for planktonic cells to adjust their buoyancy. In an environment where light and nutrients are often spatially separated, vertical adjustment relative to the water surface may be a competitive strategy to gain access to nutrients at depth (Doblin et al, 2006;Villareal et al, 2014).…”