Uphill energy transfer in photosystem I from Chlamydomonas reinhardtii. Time-resolved fluorescence measurements at 77 K

Abstract

Energetic properties of chlorophylls in photosynthetic complexes are strongly modulated by their interaction with the protein matrix and by inter-pigment coupling. This spectral tuning is especially striking in photosystem I (PSI) complexes that contain low-energy chlorophylls emitting above 700 nm. Such low-energy chlorophylls have been observed in cyanobacterial PSI, algal and plant PSI-LHCI complexes, and individual light-harvesting complex I (LHCI) proteins. However, there has been no direct evidence of their presence in algal PSI core complexes lacking LHCI. In order to determine the lowest-energy states of chlorophylls and their dynamics in algal PSI antenna systems, we performed time-resolved fluorescence measurements at 77 K for PSI core and PSI-LHCI complexes isolated from the green alga Chlamydomonas reinhardtii. The pool of low-energy chlorophylls observed in PSI cores is generally smaller and less red-shifted than that observed in PSI-LHCI complexes. Excitation energy equilibration between bulk and low-energy chlorophylls in the PSI-LHCI complexes at 77 K leads to population of excited states that are less red-shifted (by ~ 12 nm) than at room temperature. On the other hand, analysis of the detection wavelength dependence of the effective trapping time of bulk excitations in the PSI core at 77 K provided evidence for an energy threshold at ~ 675 nm, above which trapping slows down. Based on these observations, we postulate that excitation energy transfer from bulk to low-energy chlorophylls and from bulk to reaction center chlorophylls are thermally activated uphill processes that likely occur via higher excitonic states of energy accepting chlorophylls.

The structure of a red-shifted photosystem I reveals a red site in the core antenna

“…One of the conserved features of PSI is the existence of a small number of “red” or low-energy Chls, defined as Chls with an absorption maximum at longer wavelengths than P700 5 – 9 . The presence of red sites necessitates uphill energy transfer steps as part of the function of PSI and this is why this group of Chls plays a major part in determining the rate of EET in the PSI antenna 6 , 10 – 12 .…”

Recycling of energy dissipated as heat accounts for high activity of Photosystem II

“…It is, therefore, possible that the thermally-driven up-conversion also operates independently in this photosystem. Moreover, the thermally-driven up-conversion has been recently shown to operate efficiently in isolated PSI 32 . This can lead to a more general conclusion that thermally-driven up-conversion is a common mechanism in the photosynthetic apparatus and potentially important for the process of photosynthesis.…”

Light quality, oxygenic photosynthesis and more

“…Kiang et al (2007a) proposed several rules regarding where the photosynthetic pigments would peak in absorbance, and assumed that, most probably, these would account for the so-called 'green bump' (also known as 'green trough') in land plants, which is due to their relatively lower absorptance for the green light. While specific absorption wavelengths of the RCs were not predicted from the available data, Kiang et al (2007a) explained the excitation energy transfer kinetics from the LHCs to the RCs, by pointing out that even if the resonance excitation energy transfer (the Förster mechanism) toward the red is the dominant mechanism of light harvesting and energy trapping, the light energy absorbed at wavelengths longer than of the RCs (i.e., by the so-called 'red' Chls, or Chls d and f) can still be transferred uphill to the RCs (Jennings et al 2003, Giera et al 2018, Kosugi et al 2020, Tros et al 2021).…”

“…We note that PSI contains, in addition to a large fraction of Chl a molecules with broad absorption peaks in the 680-685 nm region, about 3-10% Chl a molecules that absorb above 700 nm, the so-called red or lowenergy Chls (see e.g., Jennings et al 2003, Croce et al 2007, Russo et al 2021, for land plants; Giera et al 2018, Santabarbara et al 2020, for algae; Gobets and van Grondelle 2001, Karapetyan et al 2006Karapetyan et al , 2014. The existence of 'red' Chls was first observed by Litvin and Krasnovsky (1957) and by Brody (1958) (also see Govindjee 1963).…”