Consumption of oxygen by astaxanthin biosynthesis: A protective mechanism against oxidative stress in Haematococcus pluvialis (Chlorophyceae)

Abstract

Haematococcus pluvialis, a unicellular green microalga, experiences photooxidative stress when exposed to excess photon flux density (PFD) relative to the capacity of photosynthesis, and particularly under other adverse environmental conditions (e.g., nutrient depletion, salinity, and excess heavy metals). Under stress, Haematococcus cells synthesize and accumulate large amounts of the secondary carotenoid astaxanthin stored in cytosolic lipid bodies. In this study, the transcriptional expression of five astaxanthin biosynthesis genes and two plastid terminal oxidase (PTOX) genes either in high PFD or in the presence of excessive sodium acetate and/or iron was determined by real-time reverse transcription PCR, and astaxanthin accumulation was measured by HPLC. Photosynthetic oxygen evolution, lipid peroxidation, and cell mortality were also investigated under these stress conditions. Our results indicate that the astaxanthin biosynthesis pathway may consume as much as 9.94% of the molecular oxygen evolved from photosynthesis under stress via at least two distinct routes: (1) extensive oxygen-dependent processes leading to astaxanthin formation, and (2) conversion of molecular oxygen into water using electrons derived from carotenogenic desaturation steps to PTOX via the photosynthetic plastoquinone (PQ) pool. Reduction of reactive oxygen species (ROS) production by reducing subcellular molecular oxygen substrates through the astaxanthin biosynthesis pathway may represent a novel protective mechanism to cope with oxidative stress. Reoxidation of the PQ pool by PTOX may further reduce photosynthetic electron transport chain-induced ROS formation.