Comparison of two Phaeodactylum tricornutum ecotypes under nitrogen starvation and resupply reveals distinct lipid accumulation strategies but a common degradation process

Victor Murison; Josiane Hérault; Martine Côme; Sabrina Guinio; Alexis Lebon; Christophe Chamot; Magalie Bénard; Ludovic Galas; Benoît Schoefs; Justine Marchand; Muriel Bardor; Lionel Ulmann

doi:10.3389/fpls.2023.1257500

Comparison of two Phaeodactylum tricornutum ecotypes under nitrogen starvation and resupply reveals distinct lipid accumulation strategies but a common degradation process

Front Plant Sci. 2023 Sep 22:14:1257500. doi: 10.3389/fpls.2023.1257500. eCollection 2023.

Affiliations

¹ Biology of Organisms, Stress, Health and Environment, IUT Département Génie Biologique, Le Mans Université, IUML-FR 3473 CNRS, Laval, France.
² Université de Rouen Normandie, INSERM, CNRS, HeRacLeS US51 UAR2026, PRIMACEN, Rouen, France.
³ Biology of Organisms, Stress, Health and Environment, UFR Sciences et Techniques, Le Mans Université, IUML-FR 3473 CNRS, Le Mans, France.
⁴ Université de Rouen Normandie, Laboratoire GlycoMEV UR4358, SFR Normandie Végétal FED 4277, Innovation Chimie Carnot, Rouen, France.

Abstract

Introduction: Phaeodactylum tricornutum is a model species frequently used to study lipid metabolism in diatoms. When exposed to a nutrient limitation or starvation, diatoms are known to accumulate neutral lipids in cytoplasmic lipid droplets (LDs). Those lipids are produced partly de novo and partly from the recycle of plastid membrane lipids. Under a nitrogen resupply, the accumulated lipids are catabolized, a phenomenon about which only a few data are available. Various strains of P. tricornutum have been isolated around the world that may differ in lipid accumulation patterns.

Methods: To get further information on this topic, two genetically distant ecotypes of P. tricornutum (Pt1 and Pt4) have been cultivated under nitrogen deprivation during 11 days followed by a resupply period of 3 days. The importance of cytoplasmic LDs relative to the plastid was assessed by a combination of confocal laser scanning microscopy and cell volume estimation using bright field microscopy pictures.

Results and discussion: We observed that in addition to a basal population of small LDs (0.005 μm³ to 0.7 μm³) present in both strains all along the experiment, Pt4 cells immediately produced two large LDs (up to 12 μm³ after 11 days) while Pt1 cells progressively produced a higher number of smaller LDs (up to 7 μm³ after 11 days). In this work we showed that, in addition to intracellular available space, lipid accumulation may be limited by the pre-starvation size of the plastid as a source of membrane lipids to be recycled. After resupplying nitrogen and for both ecotypes, a fragmentation of the largest LDs was observed as well as a possible migration of LDs to the vacuoles that would suggest an autophagic degradation. Altogether, our results deepen the understanding of LDs dynamics and open research avenues for a better knowledge of lipid degradation in diatoms.

Keywords: Phaeodactylum; chloroplast; diatom; lipid catabolism; lipid droplet; nitrogen; stress.

Grants and funding

The authors declare financial support was received for the research, authorship, and/or publication of this article. VM was a recipient of a PhD fellowship from the Collectivités Locales Mayennaises.