New insights into the photochemistry of carotenoid spheroidenone in light-harvesting complex 2 from the purple bacterium Rhodobacter sphaeroides

Dariusz M. Niedzwiedzki,Dewey Holten,Preston L. Dilbeck,Elizabeth C. Martin,Qun Tang,C. Neil Hunter,David F. Bocian

doi:10.1007/s11120-016-0322-2

Abstract

Light-harvesting complex 2 (LH2) from the semi-aerobically grown purple phototrophic bacterium Rhodobacter sphaeroides was studied using optical (static and time-resolved) and resonance Raman spectroscopies. This antenna complex comprises bacteriochlorophyll (BChl) a and the carotenoid spheroidenone, a ketolated derivative of spheroidene. The results indicate that the spheroidenone-LH2 complex contains two spectral forms of the carotenoid: (1) a minor, “blue” form with an S2 (11Bu+) spectral origin band at 522 nm, shifted from the position in organic media simply by the high polarizability of the binding site, and (2) the major, “red” form with the origin band at 562 nm that is associated with a pool of pigments that more strongly interact with protein residues, most likely via hydrogen bonding. Application of targeted modeling of excited-state decay pathways after carotenoid excitation suggests that the high (92%) carotenoid-to-BChl energy transfer efficiency in this LH2 system, relative to LH2 complexes binding carotenoids with comparable double-bond conjugation lengths, derives mainly from resonance energy transfer from spheroidenone S2 (11Bu+) state to BChl a via the Qx state of the latter, accounting for 60% of the total transfer. The elevated S2 (11Bu+) → Qx transfer efficiency is apparently associated with substantially decreased energy gap (increased spectral overlap) between the virtual S2 (11Bu+) → S0 (11Ag−) carotenoid emission and Qx absorption of BChl a. This reduced energetic gap is the ultimate consequence of strong carotenoid–protein interactions, including the inferred hydrogen bonding.

Highlights

Carotenoids are a class of chemical compounds that are naturally synthesized by photosynthetic organisms
The results indicate that the spheroidenone-Light-harvesting complex 2 (LH2) complex contains two spectral forms of the carotenoid: (1) a minor, ‘‘blue’’ form with an S2 (11Bu?) spectral origin band at 522 nm, shifted from the position in organic media by the high polarizability of the binding site, and (2) the major, ‘‘red’’ form with the origin band at 562 nm that is associated with a pool of pigments that more strongly interact with protein residues, most likely via hydrogen bonding
The carotenoid absorption bands are well resolved for the spheroidene-LH2 complex, with three vibronic peaks at 511, 478, and 451 nm at room temperature (RT)

Summary

Introduction

Carotenoids are a class of chemical compounds that are naturally synthesized by photosynthetic organisms. $ -) (Christensen 1999) The energies of both the S1 and S2 excited states depend on carbon–carbon double-bond (C=C) conjugation length (NC=C); the more extended the p-electron system of the carotenoid, the lower the energies of its excited states. Photosynthetic purple bacteria produce a subclass of the molecules commonly referred to as open-chain carotenoids and incorporate them into key photosynthetic machinery such as light-harvesting (LH) complexes and reaction centers. Elongation of conjugation to NC=C = 11 (e.g., rhodopin or lycopene) causes a substantial drop in the UCar?BChl efficiency to *50–60% (Angerhofer et al 1995; Billsten et al 2002; Cong et al 2008; Frank and Cogdell 1996; Garcia-Asua et al 2002)

Methods

Results

Discussion

Conclusion