Abstract
Dinoflagellates are important contributors to the marine phytoplankton and global carbon fixation, but are also infamous for their ability to form the spectacular harmful algal blooms called red tides. While blooms are often associated with high available nitrogen, there are instances where they are observed in oligotrophic environments. In order to maintain their massive population in conditions of nitrogen limitation, dinoflagellates must have evolved efficient adaptive mechanisms. Here we report the physiological responses to nitrogen deprivation in Lingulodinium polyedrum. We find that this species reacts to nitrogen stress, as do most plants and microalgae, by stopping cell growth and diminishing levels of internal nitrogen, in particular in the form of protein and chlorophyll. Photosynthesis is maintained at high levels for roughly a week following nitrate depletion, resulting in accumulated photosynthetic products in the form of starch. During the second week, photosynthesis rates decrease due to a reduction in the number of chloroplasts and the accumulation of neutral lipid droplets. Surprisingly, the starch granules and lipid droplets are seen to accumulate at opposite poles of the cell. Lastly, we observe that cells acclimated to nitrogen-depleted conditions resume normal growth after addition of inorganic nitrogen, but are able to maintain high cell densities far longer than cells grown continuously in nitrogen-replete conditions.
Highlights
Nitrogen (N) is an essential nutrient for all living organisms as it is required for biosynthesis of proteins and nucleic acids
Strategies allowing blooms to deal with N stress might appear counterintuitive, as natural and anthropogenic N addition rather than N deprivation is a factor often associated with harmful algal blooms (HAB) [3,4]
We show that Lingulodinium polyedrum cultures with cell densities similar to those observed in blooming populations in the field (,107 cells L21), are able to survive and maintain these elevated cell densities for more than 2 weeks if previously acclimated to N-deplete conditions (Fig. 1) [30]
Summary
Nitrogen (N) is an essential nutrient for all living organisms as it is required for biosynthesis of proteins and nucleic acids. In some cases dense blooms can form and persist in oligotrophic environments where the measured inorganic N supply would seem to be insufficient to support their biomass, as was observed for Karenia brevis in the West Florida Shelf [5] In this particular example it was proposed that organic N coming from decaying fish killed by the HAB explained the persistence of the dinoflagellate populations [5,6]. Another possibility is that acclimation mechanisms triggered by N deprivation during a bloom could allow the dinoflagellates to maintain bloom-density population levels until new N becomes available. Testing this hypothesis in the environment would be difficult, because of the complex interplay between biotic and abiotic factors involved in bloom dynamics [4]
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