Oligomerization and pigmentation dependent excitation energy transfer in fucoxanthin–chlorophyll proteins

Abstract

The ultrafast carotenoid to chlorophyll a energy transfer dynamics of the isolated fucoxanthin-chlorophyll proteins FCPa and FCPb from the diatom Cyclotella meneghiniana was investigated in a comprehensive study using transient absorption in the visible and near infrared spectral region as well as static fluorescence spectroscopy. The altered oligomerization state of both antenna systems results in a more efficient energy transfer for FCPa, which is also reflected in the different chlorophyll a fluorescence quantum yields. We therefore assume an increased quenching in the higher oligomers of FCPb. The influence of the carotenoid composition was investigated using FCPa and FCPb samples grown under different light conditions and excitation wavelengths at the blue (500nm) and red (550nm) wings of the carotenoid absorption. The different light conditions yield in altered amounts of the xanthophyll cycle pigments diadinoxanthin and diatoxanthin. Since no significant dynamic changes are observed for high light and low light samples, the contribution of the xanthophyll cycle pigments to the energy transfer is most likely negligible. On the contrary, the observed dynamics change drastically for the different excitation wavelengths. The analyses of the decay associated spectra of FCPb suggest an altered energy transfer pathway. For FCPa even an additional time constant was found after excitation at 500nm. It is assigned to the intrinsic lifetime of either the xanthophyll cycle carotenoids or more probable the blue absorbing fucoxanthins. Based on our studies we propose a detailed model explaining the different excitation energy transfer pathways in FCPa.

Evidence for the Existence of One Antenna-Associated, Lipid-Dissolved and Two Protein-Bound Pools of Diadinoxanthin Cycle Pigments in Diatoms

“…These pigments are visible in the fluorescence excitation spectra, which means that they act as accessory pigments in the peripheral FCP. FCPb complexes also contain protein-bound Ddx pigments, but in a much lower amount compared with FCPa (Gundermann and Bü chel, 2008;Gildenhoff et al, 2010). Importantly, in P. tricornutum, protein-bound Ddx cycle pigments are also present in the FCP (data not shown).…”

“…Thus, a quantification of the protein-bound Ddx cycle pigment pool was not possible. However, several pigment determinations were performed before with FCPs, which were isolated with anion-exchange chromatography or a two-step purification protocol using Suc gradient centrifugation in combination with anion-exchange chromatography (Beer et al, 2006;Gundermann and Bü chel, 2008;Gildenhoff et al, 2010;Premvardhan et al, 2010). All these purifications have in common that the Ddx cycle pigment content of the isolated complexes was strongly reduced in comparison with the content of the intact cell.…”

Structure and Functional Heterogeneity of Fucoxanthin-Chlorophyll Proteins in Diatoms

“…No transfer into Chl c could be observed within the limit of the instrumentation (<100 fs), giving rise to the assumption that Fx transfers its absorbed energy directly (or via other Fx) to Chl a molecules. On the other hand this means that Chl c absorption will lead to direct transfer to Chl a (Gildenhoff et al 2010a ;Papagiannakis et al 2005 ;Premvardhan et al 2009 ).…”

“…This state is strongly coupled to the S 1 state and more generally referred to as S 1 / ICT. Indeed, the excitation energy transfer from Fx to Chl a was shown to proceed mainly via the S 1 /ICT state in FCPs (Gildenhoff et al 2010a ;Papagiannakis et al 2005 ). Stark spectroscopy reveals that upon photon absorption by Fx in solvent, a huge change in the static dipole moment of 17 D takes place, indicating photo-induced charge transfer of the Fx molecules.…”

Macro-organization and structural flexibility of the photosynthetic pigment system in diatoms

“…Ultrafast transient spectroscopy studies indicate that the energy transfer pathways within the isolated FCP are also heterogeneous (Papagiannakis et al 2005;Gildenhoff et al 2010). To gain more information about the microenvironment, more precisely about the charge-transfer properties of Fx and the changes in static dipole moments, Stark-spectroscopy measurements were performed earlier on isolated FCP complexes ).…”