Lipid droplets-vacuoles interaction promotes lipophagy in the oleaginous diatom Fistulifera solaris

Abstract

Autophagy is a highly conserved process for degrading intracellular materials in vacuoles or lysosomes, commonly found in a wide range of eukaryotes. Lipid droplets are intracellular organelles that store neutral lipids, and recent studies have shown that autophagy regulates lipid metabolism by degrading lipid droplets. While autophagy-mediated degradation of lipid droplets, called lipophagy, is recognized as one of the major lipid degradation mechanisms in eukaryotic cells, its characterization in microalgae remains incomplete. Our prior investigations established a potential connection between autophagy and lipid degradation on the oleaginous microalga (diatom) Fistulifera solaris, a candidate for microalgal biofuel production. Inhibition of lipophagy can be a promising strategy to enhance the oleaginous phenotype of this alga. However, the presence of lipophagy in this alga has not been demonstrated because the interaction between vacuoles and lipid droplets has not yet been observed. In this study, we investigated lipophagy in F. solaris by microscopy, transcriptomics, and biochemical assays. Fluorescence microscopy revealed increased vacuolar contact with lipid droplets under conditions promoting lipid degradation, and this process was hindered by autophagy inhibitors. Transmission electron microscopy showed direct fusion of vacuoles and lipid droplets, suggesting that F. solaris might have a novel type of microlipophagy. These data indicate that lipophagy may play an important role in lipid degradation in F. solaris. To our knowledge this study marks the first direct observation of lipophagy in diatoms, contributing to our understanding of lipid metabolism in this organism.