Phosphorus starvation induces the synthesis of novel lipid class diacylglyceryl glucuronide and diacylglyceryl-N,N,N-trimethylhomoserine in two species of cold-adapted microalgae Raphidonema (Chlorophyta)

Abstract

Microalgae possess diverse lipid classes as components of structural membranes and have adopted various lipid remodeling strategies involving phospholipids to cope with a phosphorus (P)-limited environment. Here, we report a unique adaptative strategy to P deficient conditions in two cold-adapted microalgae, Raphidonema monicae and Raphidonema nivale, involving the lipid class diacylglyceryl glucuronide (DGGA) and the betaine lipid diacylglyceryl-N,N,N-trimethylhomoserine. Lipidomic analyses showed that these two lipid classes were present only in trace amounts in nutrient replete conditions, whereas they significantly increased under P-starvation concomitant with a reduction in phospholipids, suggesting a physiological significance of these lipid classes to combat P-starvation. Additionally, we found two putative sulfoquinovosyldiacylglycerol (SQDG) synthases, known to be involved in DGGA synthesis in higher plants, in the draft genome of R. monicae, and compared it with SQDG synthases found in other organisms such as higher plants, Streptophyta, and Chlorophyta. DGGA has not been previously recognized in Chlorophyta, and our findings suggest that the lipid class may be present in other closely related green algae too. Thus, this study expands our knowledge on diverse lipid remodeling responses of Chlorophycean algae to adapt to low P environments.