The light-harvesting 2 (LH2) complex of purple phototrophic bacteria plays a critical role in absorbing solar energy and distributing the excitation energy. Exciton dynamics within LH2 complexes are controlled by the structural arrangement and energy levels of the bacteriochlorophyll (BChl) and carotenoid (Car) pigments. However, there is still debate over the competing light-harvesting versus energy-dissipation pathways. In this work, we compared five variants of the LH2 complex from genetically modified strains of Rhodobacter sphaeroides, all containing the same BChls but different Cars with increasing conjugation: zeta-carotene (N = 7; LH2Zeta), neurosporene (N = 9; LH2Neu), spheroidene (N = 10; LH2Spher), lycopene (N = 11; LH2Lyco), and spirilloxanthin (N = 13; LH2Spir). Absorption measurements confirmed that the Car excited-state energy decreased with increasing conjugation. Similarly, fluorescence spectra showed that the B850 BChl emission peak had an increasing red shift from LH2Zeta→(LH2Neu/LH2Spher)→LH2Lyco→LH2Spir. In contrast, time-resolved fluorescence and ultrafast transient absorption (fs-TA) revealed similar excited-state lifetimes (∼1 ns) for all complexes except LH2Spir (∼0.7 ns). From fs-TA analysis, an additional ∼7 ps nonradiative dissipation step from B850 BChl was observed for LH2Zeta. Further, singlet-singlet and singlet-triplet annihilation studies showed a ∼50% average fluorescence lifetime reduction in LH2Zeta at high laser power and high repetition rate, compared to ∼10-15% reductions in LH2Neu/LH2Spher/LH2Lyco and minimal lifetime change in LH2Spir. In LH2Zeta, the fastest decay component (<50 ps) became prominent at high repetition rates, consistent with strong singlet-triplet annihilation. Nanosecond TA measurements revealed long-lived (>40 μs) BChl triplet states in LH2Zeta and signs of damage caused by singlet oxygen, whereas other LH2s showed faster triplet quenching (∼18 ns) by Cars. These findings highlight a key design principle of LH2 complexes: the Car triplet energy must be significantly lower than the BChl triplet energy to efficiently quench BChl triplets that otherwise act as potent "trap states," causing exciton annihilation in laser-based experiments or photodamage in native membranes.

Astbury Centre for Structural Molecular Biology University of Leeds Leeds LS2 9JT United Kingdom

Department of Chemical Physics and Optics Faculty of Mathematics and Physics Charles University Prague 121 16 Czech Republic

Department of Chemistry Massachusetts Institute of Technology Cambridge Massachusetts 02139 United States

Molecular Microbiology Biochemistry to Disease School of Biosciences University of Sheffield Sheffield S10 2TN United Kingdom

Plants Photosynthesis and Soil School of Biosciences University of Sheffield Sheffield S10 2TN United Kingdom

School of Physics and Astronomy University of Leeds Leeds LS2 9JT United Kingdom

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