Cell wall and organelle modifications during nitrogen starvation in Nannochloropsis oceanica F&M-M24

Abstract

Nannochloropsis oceanica F&M-M24 is able to increase its lipid content during nitrogen starvation to more than 50% of the total biomass. We investigated the ultrastructural changes and the variation in the content of main cell biomolecules that accompany the final phase of lipid accumulation. Nitrogen starvation induced a first phase of thylakoid disruption followed by chloroplast macroautophagy and formation of lipid droplets. During this phase, the total amount of proteins decreased by one-third, while carbohydrates decreased by 12–13%, suggesting that lipid droplets were formed by remodelling of chloroplast membranes and synthesis of fatty acids from carbohydrates and amino acids. The change in mitochondrial ultrastructure suggests also that these organelles were involved in the process. The cell wall increased its thickness and changed its structure during starvation, indicating that a disruption process could be partially affected by the increase in wall thickness for biomolecules recovery from starved cells. The wall thickness in strain F&M-M24 was much lower than that observed in other strains of N. oceanica, showing a possible advantage of this strain for the purpose of biomolecules extraction. The modifications following starvation were interpreted as a response to reduction of availability of a key nutrient (nitrogen). The result is a prolonged survival in quiescence until an improvement of the environmental conditions (nutrient availability) allows the rebuilding of the photosynthetic apparatus and the full recovery of cell functions.

Comparative Proteomics Reveals Evidence of Enhanced EPA Trafficking in a Mutant Strain of Nannochloropsis oculata

“…Through glycolysis, glucose sourced from the cell wall can be oxidized to generate energy that can be diverted to FA synthesis. In a recent study, during nitrogen starvation, the N. oceanica cell wall altered from two layers with a thickness of 32.9 nm to a one-layer cell wall with a thickness of 37.8 nm ( Roncaglia et al, 2021 ). This implied that the cell wall degradation might also contribute to FA synthesis.…”

Production of a viral surface protein in Nannochloropsis oceanica for fish vaccination against infectious pancreatic necrosis virus

“…All these organelles are typical for Nannochloropsis, if cultured under standard growth conditions (Fig. S5a, Roncaglia et al 2021). In both transformants, however, the small vacuoles often contained short, regular, and tightly packed tubules that were stained intensively dark (Fig.…”

“…Such structures have been previously described in N. oceanica and other Eustigmatophytes, where they specifically occurred upon nitrogen starvation. Most likely, these tubules originate from thylakoid degradation as a consequence of chlorophagy, followed by vacuolar degradation of photosynthetic protein complexes to amino acids (Roncaglia et al 2021 ). Typically, this process is paralleled by a reduction in algal protein content.…”

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“…Some nutrient limitation in our culture conditions might have triggered the formation of these organelles, which could serve as protein storage. 66 Finally, organelles with areas of electrondense and electron-opaque content were also observed in N. oculata by TEM, but only in the mid-exponential phase. These are possibly vacuoles containing phosphorus (electron-dense regions), as storage for future nutrient limitations.…”

“…54 Furthermore, the filaments observed in some organelles in the early stationary phase of N. oculata are reported to likely be protein filaments. 66 Roncaglia et al (2021) detected such organelles in a Nannochloropsis species (N. oceanica) grown in nitrogen-starved conditions. Some nutrient limitation in our culture conditions might have triggered the formation of these organelles, which could serve as protein storage.…”