Ca2+-regulated cyclic electron flow supplies ATP for nitrogen starvation-induced lipid biosynthesis in green alga

Abstract

We previously showed that both the linear photosynthetic electron transportation rate and the respiration rate dropped significantly during N starvation-induced neutral lipid accumulation in an oil-producing microalga, Chlorella sorokiniana, and proposed a possible role for cyclic electron flow (CEF) in ATP supply. In this study, we further exploited this hypothesis in both Chlorella sorokiniana C3 and the model green alga Chlamydomonas. We found that both the rate of CEF around photosystem I and the activity of thylakoid membrane-located ATP synthetase increased significantly during N starvation to drive ATP production. Furthermore, we demonstrated that the Chlamydomonas mutant pgrl1, which is deficient in PGRL1-mediated CEF, accumulated less neutral lipids and had reduced rates of CEF under N starvation. Further analysis revealed that Ca2+ signaling regulates N starvation-induced neutral lipid biosynthesis in Chlamydomonas by increasing calmodulin activity and boosting the expression of the calcium sensor protein that regulates Pgrl1-mediated CEF. Thus, Ca2+-regulated CEF supplies ATP for N starvation-induced lipid biosynthesis in green alga. The increased CEF may re-equilibrate the ATP/NADPH balance and recycle excess light energy in photosystems to prevent photooxidative damage, suggesting Ca2+-regulated CEF also played a key role in protecting and sustaining photosystems.

An Overview of Potential Oleaginous Microorganisms and Their Role in Biodiesel and Omega-3 Fatty Acid-Based Industries

“…It is possible to enhance the lipid content and the production of certain fatty acids in culture by applying different specific abiotic factors, although conditions that yield high lipid content might not be the most favorable for growth [138]. The best well-known strategy to achieve high lipid accumulation in oleaginous microorganisms is through nitrogen starvation [139][140][141][142][143][144][145]. Nitrogen is an essential part of the synthesis of proteins, nucleic acids, and chlorophyll, and during nitrogen limitation, microalgae undergo rapid metabolic remodeling, directing the carbon flow toward lipid production [140,144,[146][147][148][149][150][151][152][153].…”

Saturating Light Induces Sustained Accumulation of Oil in Plastidal Lipid Droplets in Chlamydomonas reinhardtii

“…PGRL1 is a major component of cyclic electron flow in C. reinhardtii and has been proposed to supply additional ATP for photosynthesis, particularly in conditions of high ATP demand (Tolleter et al, 2011;Dang et al, 2014). The PGRL1-deficient mutant (pgrl1) was reported recently to accumulate less neutral lipids under N starvation, and it was suggested that cyclic electron flow supplies ATP for lipid biosynthesis during N starvation (Chen et al, 2015). The association of PGRL1 with LDs of SLexposed cells expands its role in supplying ATP for Only proteins with two or more peptides and two or more specific spectral counts (SSCs) were retained for analyses.…”

Use of a lipid rich strain reveals mechanisms of nitrogen limitation and carbon partitioning in the haptophyte Tisochrysis lutea

“…reinhardtii and Chlorella sp. regulates N starvation-induced neutral lipid by increasing calmodulin activity [82,83]. We suggests that Ca 2+ signal transduction participates in lipid accumulation in haptophytes.…”