Metabolomic and transcriptomic analyses reveal the effects of ultraviolet radiation deprivation on Isochrysis galbana at high temperature

Abstract

The microalga Isochrysis galbana exhibits a seasonal fluctuation of biomass referred to as ‘decline’ during summer, leading to a great economic loss in the mariculture industry. In the present study, we aimed to explore the role of ultraviolet radiation (UVR) in I. galbana decline at high temperature by integrated analysis of metabolomic and transcriptomic data. The positive effects of UVR deprivation on the growth and photosynthetic activity of I. galbana were preliminarily evidenced by the increase in biomass concentration, the effective photochemical efficiency of photosystem II (PSII) (Fv′/Fm′), and oxygen evolution rate. Furthermore, we compared the contents of eight organic acids, total lipids and gene expression of I. galbana grown under natural sunlight versus UVR-deprived conditions, as well as. The contents of some tricarboxylic acid (TCA) cycle-related organic acids were higher in the UVR-deprived group. Lipidomic analysis indicated that UVR deprivation resulted in the accumulation of monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), sulfoquinovosyldiacylglycerol (SQDG), diacylglycerylcarboxyhydroxymethylcholine (DGCC), diacylglyceryl-N,N,N-trimethylhomoserine (DGTS), and lyso-lipids, while triacylglycerol (TAG) was decreased. Consistent with these results, the transcriptomic data showed that the expressions of some key genes involved in the TCA cycle and the photosynthesis pathways were clearly induced by UVR deprivation. Besides, the down-regulation of diacylglycerol O-acyltransferases (DGAT) and the up-regulation of TAG lipase collectively resulted in the lower accumulation of TAG, which was consistent with the metabolomic data. Taken together, the decline of I. galbana in summer could be explained by the disorder of a series of biological processes caused by UVR, especially the damage to photosynthesis, the slowdown of TCA cycle, and the disturbance of lipid metabolism. This study allowed us to better understand the responses of I. galbana to UVR stress and provided useful information for the cultivation of I. galbana in summer, greatly expanding our current knowledge on the genetic information of I. galbana.