Will nitrogen limitation and high CO₂ concentrations impact upon the sinking velocity of phytoplankton?

Abstract

The biological carbon pump in the ocean plays an important role in controlling atmospheric CO₂ levels. Approximately 1-3% of the yearly 50–60 Pg C of marine primary production settles in the deep ocean, where it is effectively sequestered for centuries to millennia. Central to the strength of the pump is the sinking velocity of phytoplankton cells and other organic debris. Stokes' Law indicates that the sinking velocity of a spherical cell will depend on its size and density, where larger, heavier cells will sink at a faster rate. Given that growth conditions can result in changes in cell size and macromolecular composition of phytoplankton, it might be expected that such changes could cause alterations in sinking velocity and carbon drawdown via the biological carbon pump. In the future, phytoplankton cells in the open ocean are predicted to be more subject to nutrient limitation due to enhanced stratification reducing the upwelling of nutrients. This will be driven by the warming of surface waters and an increase in the difference between the temperature of the surface and deeper ocean. Therefore the effects of nitrogen limitation on the sinking velocity of Emiliania huxleyi, a coccolithophore responsible for significant phytoplankton blooms and biological drawdown of carbon was examined. Nitrogen limitation caused changes in macromolecular composition, especially lipid content and also alters coccosphere thickness. However, the overall density of the cells remained similar, and, as a consequence, cell size was the major determinant of sinking rate with N-limited cells in exponential phase sinking more slowly than N-replete cells. Cells in stationary phase showed the reverse trend with N-limited cells sinking faster, although not as fast as N-replete cells in exponential phase. N-limited cells produced more transparent exopolymers (TEP), suggesting an increased capacity for aggregation and marine snow formation. Phytoplankton cells are also expected to be to be exposed to higher concentrations of CO₂ in the future, potentially 1000 p.p.m. by the year 2100. Therefore, the effects of high CO₂ (1000 p.p.m.) on the sinking velocity of E. huxleyi were also examined. The high CO₂ did not alter the sinking velocity of E. huxleyi during the exponential growth phase. This was because the overall size and density of cells remained similar between high-CO₂ and ambient CO₂ grown cultures. The increased CO₂ concentration did however cause cells to increase their protoplast diameter and decrease their coccosphere radius, suggesting that cells were reducing their rate of calcification and channelling excess carbon into organic matter production. The high CO₂ also caused the cells to alter their macromolecular composition, increasing significantly the concentrations of lipids, carbohydrates and proteins. At stationary phase, the high CO₂ did not increase TEP production. However, by stationary phase, CO₂ equilibrium could not be maintained, so there were no differences in CO₂ concentrations between cultures. While this finding sheds no light on the role that TEP plays in sinking, it does further highlight the positive relationship between CO₂ concentrations and TEP production. Phytoplankton cells will be exposed to many concurrent environmental changes in the future ocean. Therefore, the interactive effects of high CO₂ (1000 p.p.m.) and N-limitation on the sinking velocity of Chaetoceros didymus, a chain forming marine diatom, were examined. During the exponential growth phase, the N-limited/1000 p.p.m. CO₂ cells sank the fastest, followed by the N-replete/1000 p.p.m. CO₂ cells and then the N-limited/400 p.p.m. CO₂ cells. The N-replete/400 p.p.m. CO₂ cells sank at the slowest rate. The concentration of lipids and carbohydrates increased significantly in the N-replete/1000 p.p.m. CO₂ cells and increased further still when high CO₂ was combined with N-limitation, although this increase was not statistically significant. Despite this, there were no differences observed in density between any of the groups. It is likely, therefore, that the differences seen in sinking, during the exponential growth phase, were due to changes in the cells’ physical size, either through increased chain- or spine-length. During stationary phase, the two N-limited cultures displayed the greatest sinking velocities while the slowest average sinking velocity was again seen in the N-replete/400 p.p.m. CO₂ cells. The N-limited/400 p.p.m. CO₂ cultures increased their sinking velocity because of an increase in cell volume caused by enhanced chain formation. In contrast the N-limited/1000 p.p.m. CO₂ cells increased their sinking velocity because of an increase in density. During stationary phase, TEP concentrations increased significantly in the two high CO₂ cultures, a 5 times increase being seen in the N-limited/1000 p.p.m. CO₂ cultures. This increase in TEP suggests a high capacity for marine snow formation in the future ocean. These observations suggest that there will be changes in the efficiency of the biological carbon pump in the future, especially in areas that have increased nutrient stress caused by global climate change.