Red Light Control of β-Carotene Isomerisation to 9-cis β-Carotene and Carotenoid Accumulation in Dunaliella salina

Yanan Xu,Patricia J Harvey

doi:10.3390/antiox8050148

Abstract

Dunaliella salina is a rich source of 9-cis β-carotene, which has been identified as an important biomolecule in the treatment of retinal dystrophies and other diseases. We previously showed that chlorophyll absorption of red light photons in D. salina is coupled with oxygen reduction and phytoene desaturation, and that it increases the pool size of β-carotene. Here, we show for the first time that growth under red light also controls the conversion of extant all-trans β-carotene to 9-cis β-carotene by β-carotene isomerases. Cells illuminated with red light from a light emitting diode (LED) during cultivation contained a higher 9-cis β-carotene content compared to cells illuminated with white or blue LED light. The 9-cis/all-trans β-carotene ratio in red light treated cultures reached >2.5 within 48 h, and was independent of light intensity. Illumination using red light filters that eliminated blue wavelength light also increased the 9-cis/all-trans β-carotene ratio. With norflurazon, a phytoene desaturase inhibitor which blocked downstream biosynthesis of β-carotene, extant all-trans β-carotene was converted to 9-cis β-carotene during growth with red light and the 9-cis/all-trans β-carotene ratio was ~2. With blue light under the same conditions, 9-cis β-carotene was likely destroyed at a greater rate than all-trans β-carotene (9-cis/all-trans ratio 0.5). Red light perception by the red light photoreceptor, phytochrome, may increase the pool size of anti-oxidant, specifically 9-cis β-carotene, both by upregulating phytoene synthase to increase the rate of biosynthesis of β-carotene and to reduce the rate of formation of reactive oxygen species (ROS), and by upregulating β-carotene isomerases to convert extant all-trans β-carotene to 9-cis β-carotene.

Highlights

Carotenoids are synthesized by photosynthetic organisms for light-harvesting and for photo-protection of the pigment-protein light-harvesting complexes and photosynthetic reaction centres in the thylakoid membrane [1,2,3,4]
The occurrence of such high concentrations of 9-cis βC in D. salina is of great pharmaceutical interest. 9-cis βC has a higher antioxidant activity than all-trans βC, and may be more efficient than all-trans βC in vivo [12,13]. 9-cis βC has been proposed in treatments for retinal dystrophies, chronic plaque psoriasis and atherosclerosis and as an anti-ageing therapy [14,15,16,17,18]
We proposed a mechanism for carotenoid synthesis under red light, which involved absorption of red light photons by chlorophyll to reduce plastoquinone in photosystem II, coupled with phytoene desaturation by a plastoquinol:oxygen oxidoreductase, with oxygen as electron acceptor

Summary

Introduction

Carotenoids are synthesized by photosynthetic organisms for light-harvesting and for photo-protection of the pigment-protein light-harvesting complexes and photosynthetic reaction centres in the thylakoid membrane [1,2,3,4]. Two pools of β-carotene have been identified, which may be distinguished on the basis of geometric isomer configuration, cis or trans (Z/E), and enzyme complement. Thylakoid β-carotene consists principally of all-trans β-carotene (all-trans βC), and may be constitutively expressed; the ‘accumulated’ β-carotene, which is found in globules of lipid and proline-rich, β-carotene globule protein (the βC-plastoglobuli) in the inter-thylakoid spaces of the chloroplast, appears in high concentration of both cis/trans (Z/E) configurations, ratio ~1 [5,9,10,11]. The occurrence of such high concentrations of 9-cis βC in D. salina is of great pharmaceutical interest. A synthetic pure preparation of 9-cis βC has recently been shown to inhibit photoreceptor degeneration of eye cups from mice with a retinoid cycle genetic defect [19]

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