The Response of Nannochloropsis gaditana to Nitrogen Starvation Includes De Novo Biosynthesis of Triacylglycerols, a Decrease of Chloroplast Galactolipids, and Reorganization of the Photosynthetic Apparatus

Abstract

Microalgae of the genus Nannochloropsis are capable of accumulating triacylglycerols (TAGs) when exposed to nutrient limitation (in particular, nitrogen [N]) and are therefore considered promising organisms for biodiesel production. Here, after nitrogen removal from the medium, Nannochloropsis gaditana cells showed extensive triacylglycerol accumulation (38% TAG on a dry weight basis). Triacylglycerols accumulated during N deprivation harbored signatures, indicating that they mainly stemmed from freshly synthesized fatty acids, with a small proportion originating from a recycling of membrane glycerolipids. The amount of chloroplast galactoglycerolipids, which are essential for the integrity of thylakoids, decreased, while their fatty acid composition appeared to be unaltered. In starved cells, galactolipids were kept at a level sufficient to maintain chloroplast integrity, as confirmed by electron microscopy. Consistently, N-starved Nannochloropsis cells contained less photosynthetic membranes but were still efficiently performing photosynthesis. N starvation led to a modification of the photosynthetic apparatus with a change in pigment composition and a decrease in the content of all the major electron flow complexes, including photosystem II, photosystem I, and the cytochrome b 6 f complex. The photosystem II content was particularly affected, leading to the inhibition of linear electron flow from water to CO 2 . Such a reduction, however, was partially compensated for by activation of alternative electron pathways, such as cyclic electron transport. Overall, these changes allowed cells to modify their energetic metabolism in order to maintain photosynthetic growth.

A biorefinery for Nannochloropsis: Induction, harvesting, and extraction of EPA-rich oil and high-value protein

“…Nevertheless, the decrease in the other lipid classes is not equivalent to the increase in the content of the neutral lipids. This observation implies that, aside from the rearrangement of some polar lipids to form neutral lipids, de novo fatty acid synthesis is also induced (Martin et al, 2014;Simionato et al, 2013).…”

“…Most of these neutral lipids are triacylglycerides (TAGs); however, there are notable decreases in the other lipid classes (Martin et al, 2014;Simionato et al, 2013). Nevertheless, the decrease in the other lipid classes is not equivalent to the increase in the content of the neutral lipids.…”

“…F&M-M24. Simionato et al (2013) reported a large increase in the lipid content from 70 to 380 µg/mg dry weight of N. gaditana, while Fakhry and El Maghraby (2015) presented a 61% increase in lipid productivity of Nannochloropsis salina due to nitrogen starvation.…”

The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii

“…Until recently, studies of nutrient limitation in microalgae have focused on the effects seen one to several days after deprivation (Wykoff et al, 1998;Moseley et al, 2002;Urzica et al, 2013) when oil accumulation rates are high Li et al, 2010;Miller et al, 2010;Philipps et al, 2012;Simionato et al, 2013;Yang et al, 2013) and photosynthetic functions are already substantially diminished. Here, we focus on the induction phase to investigate the transition into a nutrient-deprived, oil-accumulating state and the regulation of photosynthesis during that transition.…”

“…Photosynthetic yields decrease during N deprivation, even under phototrophic conditions where cells are entirely dependent upon photosynthesis (Philipps et al, 2012;Simionato et al, 2013). Chlorophyll (Chl) fluorescence, which is sensitive to environmental changes and stress conditions that induce alterations in photosynthetic components (Iwai et al, 2008), can monitor the efficiency of linear electron flow (Baker et al, 2007) and has indicated that in N. oceanica (Simionato et al, 2013) and other algae, including C. reinhardtii (Berges et al, 1996;Li et al, 2010;Blaby et al, 2013), photosynthetic efficiency falls after N deprivation. Photosynthetically driven metabolic fluxes can also be probed by supplying 13 C-labeled bicarbonate/CO 2 and quantifying 13 C incorporation into metabolite pools (Shastri and Morgan, 2007;Feng et al, 2010;Young et al, 2011).…”