Efficient light-harvesting using non-carbonyl carotenoids: Energy transfer dynamics in the VCP complex from Nannochloropsis oceanica

Abstract

Violaxanthin-chlorophyll a protein (VCP) from Nannochloropsis oceanica is a Chl a-only member of the LHC family of light-harvesting proteins. VCP binds carotenoids violaxanthin (Vio), vaucheriaxanthin (Vau), and vaucheriaxanthin-ester (Vau-ester). Here we report on energy transfer pathways in the VCP complex. The overall carotenoid-to-Chla energy transfer has efficiency over 90%. Based on their energy transfer properties, the carotenoids in VCP can be divided into two groups; blue carotenoids with the lowest energy absorption band around 480nm and red carotenoids with absorption extended up to 530nm. Both carotenoid groups transfer energy efficiently from their S2 states, reaching efficiencies of ~70% (blue) and ~60% (red). The S1 pathway, however, is efficient only for the red carotenoid pool for which two S1 routes characterized by 0.33 and 2.4ps time constants were identified. For the blue carotenoids the S1-mediated pathway is represented only by a minor route likely involving a hot S1 state. The relaxed S1 state of blue carotenoids decays to the ground state within 21ps. Presence of a fraction of non-transferring red carotenoids with the S1 lifetime of 13ps indicates some specific carotenoid-protein interaction that must shorten the intrinsic S1 lifetime of Vio and/or Vau whose S1 lifetimes in methanol are 26 and 29ps, respectively. The VCP complex from N. oceanica is the first example of a light-harvesting complex binding only non-carbonyl carotenoids with carotenoid-to-chlorophyll energy transfer efficiency over 90%.

An algal enzyme required for biosynthesis of the most abundant marine carotenoids

“…The major allenic carotenoid species in eustigmatophytes are acyl esters of vaucheriaxanthin, which is presumably synthesized from the same biosynthetic precursors as fucoxanthin (11,13). However, the amount of vaucheriaxanthin esters and their contribution to light harvesting in eustigmatophyte algae is limited (22,23), suggesting that the loss of these carotenoids will have less marked consequences than the loss of fucoxanthin for diatoms. We therefore used the eustigmatophyte alga N. oceanica to generate mutants by random insertional mutagenesis and screened the resulting mutant library for clones with altered chlorophyll fluorescence properties, indicating an altered composition of photosynthetic pigments (24,25).…”

Optimum Production Conditions, Purification, Identification, and Antioxidant Activity of Violaxanthin from Microalga Eustigmatos cf. polyphem (Eustigmatophyceae)

“…The eustigmatophycean microalgae lack chlorophylls b and c , and they mainly contain chlorophyll a , violaxanthin, vaucheriaxanthin ester, and β-carotene as photosynthetic pigments [ 20 ]. Violaxanthin is the dominant carotenoid that usually combines with chlorophyll a and apoprotein to form violaxanthin-chorophyll- a -binding protein (VCP) complexes in the thylakoids of chloroplast, and takes part in light harvesting [ 21 , 22 ]. Violaxanthin is a structural component of the xanthophyll cycle that protects the photosynthetic apparatus against an excess of light via non-photochemical fluorescence quenching [ 23 ].…”

Chlorophyll–carotenoid excitation energy transfer and charge transfer in Nannochloropsis oceanica for the regulation of photosynthesis

“…Recently, N. oceanica has attracted growing scientific and industrial interest due to its ability to accumulate high levels of polyunsaturated fatty acids and its high growth rate (24)(25)(26). Unlike land plants and green algae, its LHCs bind only Chl a and the carotenoids violaxanthin, antheraxanthin, and zeaxanthin (Vio-Anth-Zea) and vaucheriaxanthin (27,28). This relatively simple pigment composition allows us to study qE mechanisms in a less complex system.…”