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

• The VCP complex binds violaxanthin, vaucheriaxanthin and Chl a.
• High (> 90%) carotenoid–Chl energy transfer efficiency
• Two carotenoid pools absorbing in the blue and red part of carotenoid absorption
• First highly-efficient system utilizing only non-carbonyl carotenoids

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 480 nm and red carotenoids with absorption extended up to 530 nm. 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 2.4 ps 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 21 ps. Presence of a fraction of non-transferring red carotenoids with the S1 lifetime of 13 ps 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 29 ps, 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%.