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The dinoflagellate Lingulodinium polyedrum responds to N depletion by a polarized deposition of starch and lipid bodies.

Dagenais Bellefeuille S, Dorion S, Rivoal J, Morse D - PLoS ONE (2014)

Bottom Line: While blooms are often associated with high available nitrogen, there are instances where they are observed in oligotrophic environments.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.

View Article: PubMed Central - PubMed

Affiliation: Institut de Recherche en Biologie Végétale, Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

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.

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TAGs accumulate in N stressed cells.A) Neutral lipid levels. Results are mean ± SE (n = 3). Statistically different results (p<0.05) are marked with a different letter (Analysis of variance). FW; Fresh weight. DIC, Nile red-stained lipid bodies and merged images of day 0 (B–D), day 7 (E–G) and day 14 cells (H–J). All cells were pictured from a ventral view. Lipid bodies were most predominant in the anterior part of the cells.
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pone-0111067-g006: TAGs accumulate in N stressed cells.A) Neutral lipid levels. Results are mean ± SE (n = 3). Statistically different results (p<0.05) are marked with a different letter (Analysis of variance). FW; Fresh weight. DIC, Nile red-stained lipid bodies and merged images of day 0 (B–D), day 7 (E–G) and day 14 cells (H–J). All cells were pictured from a ventral view. Lipid bodies were most predominant in the anterior part of the cells.

Mentions: Neutral lipids, particularly triacylglycerols (TAGs), also accumulate in N-deplete Lingulodinium (Fig. 6). TAG levels in cell extracts, measured using Nile red, were ∼2 times and ∼10 times higher than in cells at day 0 after 7 and 14 days in f/2-N, respectively (Fig. 6A). Again, this form of C storage can be visualized in cells microscopically (Fig. 6B–J). Abundance and size of lipid bodies clearly increased with the duration of N stress (Fig. 6C, F, I). However, in sharp contrast to the starch granules, TAGs accumulated preferentially at the anterior end of the cell (Fig. 6D, G, J).


The dinoflagellate Lingulodinium polyedrum responds to N depletion by a polarized deposition of starch and lipid bodies.

Dagenais Bellefeuille S, Dorion S, Rivoal J, Morse D - PLoS ONE (2014)

TAGs accumulate in N stressed cells.A) Neutral lipid levels. Results are mean ± SE (n = 3). Statistically different results (p<0.05) are marked with a different letter (Analysis of variance). FW; Fresh weight. DIC, Nile red-stained lipid bodies and merged images of day 0 (B–D), day 7 (E–G) and day 14 cells (H–J). All cells were pictured from a ventral view. Lipid bodies were most predominant in the anterior part of the cells.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4219697&req=5

pone-0111067-g006: TAGs accumulate in N stressed cells.A) Neutral lipid levels. Results are mean ± SE (n = 3). Statistically different results (p<0.05) are marked with a different letter (Analysis of variance). FW; Fresh weight. DIC, Nile red-stained lipid bodies and merged images of day 0 (B–D), day 7 (E–G) and day 14 cells (H–J). All cells were pictured from a ventral view. Lipid bodies were most predominant in the anterior part of the cells.
Mentions: Neutral lipids, particularly triacylglycerols (TAGs), also accumulate in N-deplete Lingulodinium (Fig. 6). TAG levels in cell extracts, measured using Nile red, were ∼2 times and ∼10 times higher than in cells at day 0 after 7 and 14 days in f/2-N, respectively (Fig. 6A). Again, this form of C storage can be visualized in cells microscopically (Fig. 6B–J). Abundance and size of lipid bodies clearly increased with the duration of N stress (Fig. 6C, F, I). However, in sharp contrast to the starch granules, TAGs accumulated preferentially at the anterior end of the cell (Fig. 6D, G, J).

Bottom Line: While blooms are often associated with high available nitrogen, there are instances where they are observed in oligotrophic environments.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.

View Article: PubMed Central - PubMed

Affiliation: Institut de Recherche en Biologie Végétale, Département de Sciences Biologiques, Université de Montréal, Montréal, Québec, Canada.

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.

Show MeSH
Related in: MedlinePlus