A photosynthetic antenna complex foregoes unity carotenoid-to-bacteriochlorophyll energy transfer efficiency to ensure photoprotection.

Abstract

Carotenoids play a number of important roles in photosynthesis, primarily providing light-harvesting and photoprotective energy dissipation functions within pigment-protein complexes. The carbon-carbon double bond (C=C) conjugation length of carotenoids (<i>N</i>), generally between 9 and 15, determines the carotenoid-to-(bacterio)chlorophyll [(B)Chl] energy transfer efficiency. Here we purified and spectroscopically characterized light-harvesting complex 2 (LH2) from <i>Rhodobacter sphaeroides</i> containing the <i>N</i> = 7 carotenoid zeta (ζ)-carotene, not previously incorporated within a natural antenna complex. Transient absorption and time-resolved fluorescence show that, relative to the lifetime of the S₁ state of ζ-carotene in solvent, the lifetime decreases ∼250-fold when ζ-carotene is incorporated within LH2, due to transfer of excitation energy to the B800 and B850 BChls <i>a</i> These measurements show that energy transfer proceeds with an efficiency of ∼100%, primarily via the S₁ → Q_x route because the S₁ → S₀ fluorescence emission of ζ-carotene overlaps almost perfectly with the Q_x absorption band of the BChls. However, transient absorption measurements performed on microsecond timescales reveal that, unlike the native <i>N</i> ≥ 9 carotenoids normally utilized in light-harvesting complexes, ζ-carotene does not quench excited triplet states of BChl <i>a</i>, likely due to elevation of the ζ-carotene triplet energy state above that of BChl <i>a</i> These findings provide insights into the coevolution of photosynthetic pigments and pigment-protein complexes. We propose that the <i>N</i> ≥ 9 carotenoids found in light-harvesting antenna complexes represent a vital compromise that retains an acceptable level of energy transfer from carotenoids to (B)Chls while allowing acquisition of a new, essential function, namely, photoprotective quenching of harmful (B)Chl triplets.