An unusual pathway of excitation energy deactivation in carotenoids: Singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna

doi:10.1073/pnas.051501298

An unusual pathway of excitation energy deactivation in carotenoids: Singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna

^*Department of Biophysics and Physics of Complex Systems, Division of Physics and Astronomy, Faculty of Sciences, Vrije Universiteit, 1081 HV Amsterdam, The Netherlands; ^§Department of Chemistry, University of California, and Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720; ^¶Division of Biochemistry and Molecular Biology, University of Glasgow, Glasgow G128QQ, United Kingdom; and ^‖Department of Molecular Biology and Biochemistry, Rutgers University, Piscataway, NJ 08854

Edited by Robin M. Hochstrasser, University of Pennsylvania, Philadelphia, PA, and approved December 27, 2000 (received for review October 23, 2000)

Abstract

Carotenoids are important biomolecules that are ubiquitous in nature and find widespread application in medicine. In photosynthesis, they have a large role in light harvesting (LH) and photoprotection. They exert their LH function by donating their excited singlet state to nearby (bacterio)chlorophyll molecules. In photosynthetic bacteria, the efficiency of this energy transfer process can be as low as 30%. Here, we present evidence that an unusual pathway of excited state relaxation in carotenoids underlies this poor LH function, by which carotenoid triplet states are generated directly from carotenoid singlet states. This pathway, operative on a femtosecond and picosecond timescale, involves an intermediate state, which we identify as a new, hitherto uncharacterized carotenoid singlet excited state. In LH complex-bound carotenoids, this state is the precursor on the reaction pathway to the triplet state, whereas in extracted carotenoids in solution, this state returns to the singlet ground state without forming any triplets. We discuss the possible identity of this excited state and argue that fission of the singlet state into a pair of triplet states on individual carotenoid molecules constitutes the mechanism by which the triplets are generated. This is, to our knowledge, the first ever direct observation of a singlet-to-triplet conversion process on an ultrafast timescale in a photosynthetic antenna.

Footnotes

↵ † C.C.G. and J.T.M.K. contributed equally to this work.
↵ ‡ To whom reprint requests should be addressed. E-mail: klaus{at}nat.vu.nl.
This paper was submitted directly (Track II) to the PNAS office.
Abbreviations:

Car,

carotenoid;

BChl,

bacteriochlorophyll;

LH,

light harvesting;

Spx,

spirilloxanthin;

TA,

transient absorption;

SADS,

species-associated difference spectrum;

ESA,

excited-state absorption;

EET,

excitation energy transfer;

RC,

reaction center;

RT,

room temperature;

IC,

internal conversion