The role of far-red spectral states in the energy regulation of phycobilisomes

The main light-harvesting pigment-protein complex of cyanobacteria and certain algae is the phycobilisome, which harvests sunlight and regulates the flow of absorbed energy to provide the photochemical reaction centres with a constant energy throughput. At least two light-driven mechanisms of excited energy quenching in phycobilisomes have been identified: the dominant mechanism in many strains of cyanobacteria depends on the orange carotenoid protein (OCP), while the second mechanism is intrinsically available to a phycobilisome and is possibly activated faster than the former. Recent single molecule spectroscopy studies have shown that far-red (FR) emission states are related to the OCP-dependent mechanism and it was proposed that the second mechanism may involve similar states. In this study, we examined the dynamics of simultaneously measured emission spectra and intensities from a large set of individual phycobilisome complexes from Synechocystis PCC 6803. Our results suggest a direct relationship between FR spectral states and thermal energy dissipating states and can be explained by a single phycobilin pigment in the phycobilisome core acting as the site of both quenching and FR emission likely due to the presence of a charge-transfer state. Our experimental method provides a means to accurately resolve the fluorescence lifetimes and spectra of the FR states, which enabled us to quantify a kinetic model that reproduces most of the experimentally determined properties of the FR states.M.G., T.P.J.K. and R.v.G. were supported by R.v.G.'s advanced investigator grant (267333, PHOTPROT) from the European Research Council and TOP grant (700.58.305) from the Foundation of Chemical Sciences part of NWO. T.P.J.K. was additionally supported by the University of Pretoria‘s Research Development Programme (A0W679). R.v.G. gratefully acknowledges his ‘Academy Professor’ grant from the Royal Netherlands Academy of Arts and Sciences (KNAW). M.G. was additionally funded by EMBO, the Claude Leon Foundation and the University of Pretoria.http://www.elsevier.com/locate/bbamem2020-04-01hj2019Physic