The light-harvesting function of carotenoids in the cyanobacterial stress-inducible IsiA complex Rudi Berera * , Ivo H.M. van Stokkum, John T.M. Kennis, Rienk van Grondelle, Jan P. Dekker Department of Physics and Astronomy, Faculty of Sciences, VU University Amsterdam, De Boelelaan 1081, 1081 HV Amsterdam, The Netherlands article info Article history: Received 14 October 2009 In final form 19 January 2010 Available online xxxx Keywords: Carotenoids Light harvesting Ultrafast spectroscopy Cyanobacteria abstract We present a spectroscopic investigation of the light-harvesting role of carotenoids in aggregates of the IsiA pigment–protein complex of the cyanobacterium Synechocystis PCC 6803. The results show that carotenoids in IsiA transfer energy on the sub-100 fs timescale from the S 2 state to chlorophyll to about the same extent as in the related pigment–protein complexes CP43 and CP47. Selective excitation at the red edge of the S 2 absorption of the carotenoids shows that echinenone is more efficient in energy trans- fer to chlorophyll (37%) when compared to the other carotenoid species in the system (22%). Ó 2010 Elsevier B.V. All rights reserved. 1. Introduction Cyanobacteria, also known as blue green algae, are among the oldest life forms. Their ability to perform oxygenic photosynthesis is widely thought to have led several billion years ago to the con- version of a reducing atmosphere into an oxidizing one which marked the beginning of the proliferation of a variety of life forms on Earth. Cyanobacteria are extremely robust organisms found in a variety of climate conditions. They populate the oceans where they are one of the main primary producers, but are also found in fresh- water and in the extremely harsh conditions of hypersaline lakes. To the other extreme cyanobacteria can live in the desert and with- in rocks, thus in very arid conditions. They can survive in excep- tionally acidic or basic environments thus showing a tremendous capacity of adaptation. Of particular importance is their capacity to survive and thrive in environments with continuously changing iron concentration and light intensity. When exposed to iron starvation cyanobacteria start to express the IsiA gene which triggers the synthesis of the IsiA protein or CP43 0 . This protein binds on average 16 chlorophyll a molecules and four carotenoids (b-carotene, zeaxanthin and echinenone in a stoichiometry 2:1:1). IsiA forms circular aggregates (rings) of up to 18 units around the trimeric photosystem I (PSI) core complex in a first ring [1,2] and up to 25 subunits in a second ring [3]. It was estimated that IsiA increases the absorption cross section for PSI up to a factor two [4] thus working as a very efficient accessory light-harvesting antenna. It was shown that energy transfer be- tween the IsiA ring and the PSI core complex takes place on a few ps timescale [5,6]. Physiological studies, however, assigned a photoprotective role to IsiA [7], which was corroborated by ultra- fast fluorescence and absorbance-difference spectroscopy [8,9]. Thus IsiA appears to have a dual function; it functions as a light- harvesting antenna by increasing the absorption cross section of PSI, and as energy dissipator. Following our recent paper on the mechanism of energy dissipation in IsiA [9], in this manuscript we further explore the role of carotenoids in the system. The importance of carotenoids in nature is testified by their ubiquity in living organisms. In photosynthetic organisms, carote- noids are active in light harvesting, photoprotection and structure organization [10,11]. Of vital importance for the survival of the photosynthetic organisms is the role of carotenoids in photopro- tection [12]. Carotenoids quench harmful chlorophyll triplet states which are potential singlet oxygen sensitizers and are very effec- tive scavengers of singlet oxygen [11]. This capacity relies on the low-lying carotenoid triplet state whose energy is close enough to effectively quench chlorophyll triplet states and singlet oxygen. Another pivotal role of carotenoids is in the quenching of chlo- rophyll singlet excited states under conditions of excess light illu- mination, a process generally known as nonphotochemical quenching (NPQ) [13–20]. In this paper we report on the light-harvesting role of carote- noids in aggregates of the IsiA protein from the cyanobacterium Synechocystis PCC 6803. We show, by making use of femtosecond spectroscopic techniques, that carotenoid to chlorophyll energy transfer takes place on the sub-100 fs timescale and that a major role in the process is played by a red-absorbing carotenoid, most likely echinenone. 0301-0104/$ - see front matter Ó 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.chemphys.2010.01.011 * Corresponding author. Present address: Institute of Biology and Technology of Saclay, CEA, URA 2096 CNRS 91191 Gif/Yvette, France. E-mail address: rberera@few.vu.nl (R. Berera). Chemical Physics xxx (2010) xxx–xxx Contents lists available at ScienceDirect Chemical Physics journal homepage: www.elsevier.com/locate/chemphys ARTICLE IN PRESS Please cite this article in press as: R. Berera et al., Chem. Phys. (2010), doi:10.1016/j.chemphys.2010.01.011