High-Light-Induced Stress Activates Lipid Deacylation at the Sn-2 Position in the Cyanobacterium Synechocystis Sp. PCC 6803

Plant Cell Physiol. 2022 Jan 25;63(1):82-91. doi: 10.1093/pcp/pcab147.

Abstract

Cyanobacterial mutants defective in acyl-acyl carrier protein synthetase (Aas) produce free fatty acids (FFAs) because the FFAs generated by deacylation of membrane lipids cannot be recycled. An engineered Aas-deficient mutant of Synechocystis sp. PCC 6803 grew normally under low-light (LL) conditions (50 µmol photons m-2 s-1) but was unable to sustain growth under high-light (HL) conditions (400 µmol photons m-2 s-1), revealing a crucial role of Aas in survival under the HL conditions. Several-times larger amounts of FFAs were produced by HL-exposed cultures than LL-grown cultures. Palmitic acid accounted for ∼85% of total FFAs in HL-exposed cultures, while C18 fatty acids (FAs) constituted ∼80% of the FFAs in LL-grown cultures. Since C16 FAs are esterified to the sn-2 position of lipids in the Synechocystis species, it was deduced that HL irradiation activated deacylation of lipids at the sn-2 position. Heterologous expression of FarB, the FFA exporter protein of Neisseria lactamica, prevented intracellular FFA accumulation and rescued the growth defect of the mutant under HL, indicating that intracellular FFA was the cause of growth inhibition. FarB expression also decreased the 'per-cell' yield of FFA under HL by 90% and decreased the proportion of palmitic acid to ∼15% of total FFA. These results indicated that the HL-induced lipid deacylation is triggered not by strong light per se but by HL-induced damage to the cells. It was deduced that there is a positive feedback loop between HL-induced damage and lipid deacylation, which is lethal unless FFA accumulation is prevented by Aas.

Keywords: Acyl-ACP synthetase; Lipid deacylation; Photoinhibition; Toxicity to FFAs.

Publication types

  • Comparative Study

MeSH terms

  • Adaptation, Ocular / physiology
  • Cells, Cultured / radiation effects
  • Fatty Acids, Nonesterified / metabolism*
  • Gene Expression Regulation, Plant
  • Genes, Plant
  • Light / adverse effects*
  • Membrane Lipids / metabolism*
  • Mutation
  • Stress, Physiological
  • Synechocystis / genetics*
  • Synechocystis / metabolism*
  • Synechocystis / radiation effects*
  • Thiolester Hydrolases / metabolism*

Substances

  • Fatty Acids, Nonesterified
  • Membrane Lipids
  • Thiolester Hydrolases