Glutathione peroxidase 5 deficiency induces lipid metabolism regulated by reactive oxygen species in Chlamydomonas reinhardtii

Background: Reactive oxygen species (ROS) are generated incidentally during natural metabolism process of aerobic photosynthetic organisms which could be either harmful for cellular components. How ROS regulated lipid metabolism and the transcriptomes of stressed cells respond to ROS in aerobic photosynthetic organisms are unclear. Glutathione peroxidases (GPXs) detoxify hydrogen peroxide or organic hydroperoxides, which are important enzymes of the antioxidant system. So the function of GPXs matters the cellular redox state. How the lipid metabolism respond to the GPXs deficiency remains to be explored. Methods: In this study, we employed a Chlamydomonas reinhardtii gpx5 knockout mutant to examine the effects of ROS on lipid metabolism. The redox state and lipid content of the parental strain CC4348 and the gpx5 mutant were detected. Besides, the transcriptomes of CC4348 and the gpx5 mutant were sequenced before and after treatment with nitrogen-free medium to obtain genome wide respond. Then we performed the functional annotation, classification and enrichment analysis based on KEGG database for the differentially expressed genes (DEGs) before and after nitrogen deprivation of CC4348 and the gpx5 mutant. Results: In the CC4348 cells, the lipid accumulated accompanying with increasing ROS level after treatment with nitrogen-free media. However, in the gpx5 mutant, the ROS level is much higher than that in the parental strain CC4348, unexpectedly with reduced lipid accumulation. By comparing the transcriptomes of CC4348 and gpx5 mutant, we found that both CC4348 and gpx5 mutant cells displayed upregulation of transcripts related to protein, nucleic acid, carbon metabolism and chlorophyll biosynthesis, but more proportion of genes related to lipid metabolism were up-regulated in CC4348 than that in the gpx5 mutant. Conclusion: In CC4348, lipid metabolism was up-regulated with increasing ROS level. But in the gpx5 mutant, Lipid accumulation was less with higher ROS level, which was due to the inhibited lipid biosynthesis. Therefore, ROS provides dual-directional regulation of lipid metabolism induced by GPX5 in Chlamydomonas.