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Membrane lipid remodeling contributes to the environmental acclimation of plants. In the green lineage, a betaine lipid, diacylglyceryl-N,N,N-trimethylhomoserine (DGTS), is included exclusively among green algae and nonflowering plants. Here, we show that the green alga Chlorella kessleri synthesizes DGTS under phosphorus-deficient conditions through the eukaryotic pathway via the ER. Simultaneously, phosphatidylcholine and phosphatidylethanolamine, which are similar to DGTS in their zwitterionic properties, are almost completely degraded to release 18.1% cellular phosphorus, and to provide diacylglycerol moieties for a part of DGTS synthesis. This lipid remodeling system that substitutes DGTS for extrachloroplast phospholipids to lower the P-quota operates through the expression induction of the BTA1 gene. Investigation of this lipid remodeling system is necessary in a wide range of lower green plants for a comprehensive understanding of their phosphorus deficiency acclimation strategies., Oishi et al. report that the synthesis of a betaine lipid, diacylglyceryl-N,N,N-trimethylhomoserine (DGTS) in a green alga Chlorella kessleri replaces phosphatidylcholine and phosphatidylethanolamine, the two most abundant phospholipids, during phosphate deprivation. This study provides insights into the understanding of the phosphorus-deficiency acclimation strategies via lipid remodeling in lower green plants.

Triacylglycerols (TG), the major components of crop oils used for the production of food oils and biodiesel fuel, accumulate in algal species under single environmental stress conditions including nitrogen-starvation. In a freshwater green alga, Chlorella kessleri, its TG content reached 24.7% in dry cell weight in 72 h, on cultivation in 3-fold diluted seawater (1/3 SW), through the synergetic stimulating effects of hyperosmosis and nutrient-limitation. These observations would indicate the importance of combinatory stresses for strong induction of TG accumulation [Hirai et al. 2016]. We here searched for novel stresses in C. kessleri to elevate the seawater-based TG accumulation level through their additional actions. A higher light intensity (moderate light, ML) caused a small, but definite increase of TG, whereas a lowered growth temperature (LT) led to a large, but temporal increase of it until 48 h, followed by severe degradation. The decrease of TG in LT cells was abolished on simultaneous imposition of ML. C. kessleri cells were then cultured in 1/3 SW under combinatory conditions of ML/LT, the TG content consequently increasing to as high as 48.5% in dry cells. These results indicated the validity of combinatory stresses for strong induction of algal TG accumulation. As to the fatty acid composition of TG, C. kessleri was intermediate between palm and the other three major oil crops including rapeseed. The rapid and abundant accumulation of TG with fatty acid composition suitable for industrial use demonstrated the great potential of development of the industrial algal TG production system with the use of the combinatory stresses in C. kessleri. TG of C. kessleri was also characteristic to contain C18 acids as representing 81 mol% of its constituent fatty acids or 90% of fatty acids at its sn-2 position, which suggested a peculiar TG synthetic pathway in this oleaginous alga.

Chlorella kessleri accumulates triacylglycerol usable for biodiesel-fuel production to >20% dry cell weight in three days when cultured in three-fold diluted seawater, which imposes the combinatory stress of hyperosmosis and nutrients limitation. The quantitative behavior of major C-compounds, and related-gene expression patterns were investigated in Chlorella cells stressed with hyperosmosis, nutrients limitation, or their combination, to elucidate the C-metabolism for economical seawater-based triacylglycerol accumulation. Combinatory-stress cells showed repressed protein synthesis with initially accumulated starch being degraded later, the C-metabolic flow thereby being diverted to fatty acid and subsequent triacylglycerol accumulation. This C-flow diversion was induced by cooperative actions of nutrients-limitation and hyperosmosis. Semi-quantitative PCR analysis implied positive rewiring of the diverted C-flow into triacylglycerol in combinatory-stress cells through upregulation of gene expression concerning fatty acid and triacylglycerol synthesis, and starch synthesis and degradation. The information of regulatory C-metabolism will help reinforce the seawater-based triacylglycerol accumulation ability in algae including Chlorella.