Oxygen-evolving Photosystem II core complexes: a new paradigm based on the spectral identification of the charge-separating state, the primary acceptor and assignment of low-temperature fluorescence

Abstract

We review our recent low-temperature absorption, circular dichroism (CD), magnetic CD (MCD), fluorescence and laser-selective measurements of oxygen-evolving Photosystem II (PSII) core complexes and their constituent CP 4 3, CP 47 and D1/D2/cytb(559) sub-assemblies. Quantitative comparisons reveal that neither absorption nor fluorescence spectra of core complexes are simple additive combinations of the spectra of the sub-assemblies. The absorption spectrum of the D1/D2/cytb(559) component embedded within the core complex appears significantly better structured and red-shifted compared to that of the isolated sub-assembly. A characteristic MCD reduction or 'deficit' is a useful signature for the central chlorins in the reaction centre. We note a congruence of the MCD deficit spectra of the isolated D1/D2/cytb(559) sub-assemblies to their laser-induced transient bleaches associated with P 680. A comparison of spectra of core complexes prepared from different organisms helps distinguish features due to inner light-harvesting assemblies and the central reaction-centre chlorins. Electrochromic spectral shifts in core complexes that occur following low-temperature illumination of active core complexes arise from efficient charge separation and subsequent plastoquinone anion (Q(A)(-)) formation. Such measurements allow determinations of both charge-separation efficiencies and spectral characteristics of the primary acceptor, Pheo(D1). Efficient charge separation occurs with excitation wavelengths as long as 700 nm despite the illuminations being performed at 1.7 K and with an extremely low level of incident power density. A weak, homogeneously broadened, charge-separating state of PSII lies obscured beneath the CP 47 state centered at 690 nm. We present new data in the 690-760 nm region, clearly identifying a band extending to 730 nm. Active core complexes show remarkably strong persistent spectral hole-burning activity in spectral regions attributable to CP 43 and CP 47. Measurements of homogeneous hole-widths have established that, at low temperatures, excitation transfer from these inner light-harvesting assemblies to the reaction centre occurs with approximately 70-270 ps(-1) rates, when the quinone acceptor is reduced. The rate is slower for lower-energy sub-populations of an inhomogeneously broadened antenna (trap) pigment. The complex low-temperature fluorescence behaviour seen in PSII is explicable in terms of slow excitation transfer from traps to the weak low-energy charge-separating state and transfer to the more intense reaction-centre excitations near 685 nm. The nature and origin of the charge-separating state in oxygen-evolving PSII preparations is briefly discussed.

Spectral Signatures of Photosynthesis. I. Review of Earth Organisms

“…However, Krausz, et al (2005) found that there is charge separation in PS II in spinach even over the range 700-730 nm. So, uphill energy transfer is not the most productive way to obtain energy, but nonetheless the phenomenon indicates more means of light harvesting, while resonance transfer of energy toward the red is the dominant means of light harvesting and energy trapping.…”

“…Also, the Chl a primary donor of PS I has its peak absorbance at 700 nm. Significant phenomena occur in the red edge region (Krausz, et al, 2005, called it "spectral congestion" with regard to an even more detailed structural antenna minor sub-bands occur for PS I and PS II; 678.5 nm, the main sub-band for PS II; 680 nm, the location of the primary donor P680 for PS II; 682 nm, the main sub-band for PS I; and 700 nm, the primary donor P700 for PS I. The main sub-bands are actually where most of the light harvesting of the core antenna occurs.…”

Interactions between photosynthetic pigments in organisms and in model systems

“…It was possible to establish not only the presence of these carotenes but even their orientations because of the improvement in the structural X-ray method. Nevertheless, Krausz et al (2005) did not show the presence of these Cars. Cars in the organisms can play three roles: (1) they can work as light-harvesting pigments transferring the energy absorbed to Chls: 1 Car + hν → 1 Car * → 1 Chl * (1)…”

“…The mechanism responsible for their role in prevention of the damage to PS2 RC by too strong irradiation was discussed taking into account the actual distances between pigment molecules obtained in experiments (Telfer 2005). The data concerning PS2 core complexes in which the presence of these carotenes was not taken into account were recently published (Krausz et al 2005). Telfer (2005) added that one of the two β-carotenes located near PS2 RC in PS2 core structure, bound to D2 complex, is more or less parallel to the plane of membrane, whereas the other one is roughly perpendicular to the membrane plane.…”

The Chemical Problem of Energy Change: Multi-Electron Processes

“…[11] However, even with its great success, some electron transfer problems have struggled to reach a consensus through advancements of the Marcus Theory framework. Our favourite example is the primary photo-energetics of charge separation Photosystem II where difficulty arises in physically explaining the ultrafast kinetics and energy-trapping events, [12][13][14] not to mention the catalytic four-electron water oxidation chemistry. [15,16] This example also highlights our theme, the chemical problem of energy change.…”