Photophysical Consequences of Spheroidene Reconstitution in LH1 of Rsp. rubrum: Improved Energy Transfer and Altered Photoprotection.

Abstract

Carotenoids are multifunctional pigments that play indispensable roles in photosynthesis, serving both to harvest light and to safeguard the system against photo-induced damage. In purple photosynthetic bacteria, these pigments, alongside bacteriochlorophyll (BChl) a, initiate the primary photochemical process by capturing solar energy within light-harvesting (LH) complexes. The excitation energy absorbed by carotenoids is efficiently transferred to BChl a and subsequently to the reaction center, where charge separation drives energy conversion. Improving the efficiency of excitation energy transfer (EET) from carotenoids to BChl a is a promising strategy for advancing bio-inspired light-harvesting systems and artificial photosynthesis. Here, we reconstituted spheroidene, a carotenoid known to achieve ~90% EET efficiency in the LH2 complex of Rhodobacter sphaeroides strain 2.4.1, into the carotenoidless LH1 complex of Rhodospirillum (Rsp.) rubrum strain G9+. This modification was anticipated to enhance EET efficiency relative to the native LH1 complex of Rsp. rubrum strain S1. Fluorescence excitation spectroscopy confirmed an improvement in EET. Surprisingly, sub-nanosecond time-resolved absorption spectroscopy revealed the emergence of a long-lived BChl a cation, an unusual state not typically observed in native systems. This phenomenon coincided with shortened triplet lifetimes of both carotenoid and BChl a, implying altered photoprotective dynamics. These findings suggest that while spheroidene facilitates efficient energy transfer in LH1 from Rsp. rubrum, it may also perturb the native protein environment, potentially compromising photoprotection. Our study underscores the delicate balance between energy transfer and photostability, offering new insights into the design of robust and efficient artificial photosynthetic systems.