The Electronic Origin of Far‐Red‐Light‐Driven Oxygenic Photosynthesis

Abstract

Photosystem-II uses sunlight to trigger charge separation and catalyze water oxidation. Intrinsic properties of chlorophyll a pigments define a natural "red limit" of photosynthesis at � 680 nm. Nevertheless, charge separation can be triggered with far-red photons up to 800 nm, without altering the nature of lightharvesting pigments. Here we identify the electronic origin of this remarkable phenomenon using quantum chemical and multiscale simulations on a native Photosystem-II model. We find that the reaction center is preorganized for charge separation in the far-red region by specific chlorophyll-pheophytin pairs, potentially bypassing the light-harvesting apparatus. Charge transfer can occur along two distinct pathways with one and the same pheophytin acceptor (Pheo D1 ). The identity of the donor chlorophyll (Chl D1 or P D1 ) is wavelengthdependent and conformational dynamics broaden the sampling of the far-red region by the two charge-transfer states. The two pathways rationalize spectroscopic observations and underpin designed extensions of the photosynthetically active radiation limit.

Electronic Structure Effects Related to the Origin of the Remarkable Near-Infrared Absorption of Blastochloris viridis’ Light Harvesting 1-Reaction Center Complex

“…Using system 7 as a representative example, the main transitions are explained by two simultaneous electronic excitations (see Figure ), with each transition localized on each BChl- b pigment. The coexistence of both electronic transitions is equivalent to the exciton delocalization, such as the ones described by the electronic transitions in sampled system 9 (see Figure ); also, the sampled system 6 NTOs correspond to a charge transfer process between both BChl- b pigments on one of the two electronic transitions (see Figure ), with this process being involved on the red-shifting effects, like the one present on the photosystem-II oxygenic photosynthetic structure . The rest of the NTOs associated to the electronic transitions on the sampled structures are reported in the SI (Figures S2–S11).…”

“…10,11 Some organisms, such as certain species of cyanobacteria, have even evolved to adapt to low intensity light conditions rearranging their LHC structures to absorb infrared light by a well-established phenomenon known as far red light photoacclimation (FarLiP) in which paralagous subunits of PS-I and PS-II are expressed for the purpose of harvesting longer wavelengths in environments with low levels of white light, but even in these conditions, the maximum absorption is observed around 810 nm. 12,13 In the field of agrotechnology, far-red absorbing photosynthetic pigments from cyanobacteria, such as BChl-d, have been successfully included into the LHC of plants (LHC-II), without altering their overall architecture, as a crop-boosting strategy; however, the far-red absorption only shifts the maximum absorption from 672 to 699 nm (∼27 nm). 14 A few naturally occurring photosystems show a noticeable redshift with respect to the isolated pigments in solution 15,16 but none as extreme as the observed on the light harvesting 1reaction center (LH1-RC) of Blastochloris viridis, 17 whose main absorption is located at 1015 nm, more than 200 nm upward from that of bacteriochlorophyll-b (BChl-b), the main pigment present in this LH complex, which shows an absorption maximum at 795 nm in solution (MeOH).…”

“…LHCs are composed of pigments embedded in proteins in specific arrangements; these photosynthetic pigments, such as chlorophylls (Chl), bacteriochlorophylls (BChl), and carotenoids, have their main absorptions in the UV–visible range of the electromagnetic spectra, with bacteriochlorophylls being the most abundant of them . These tetrapyrrolic, Mg 2+ coordinating pigments show their main absorption bands on the red region of visible light ranging from 760 to 800 nm in solution; however, in their solvated natural configurations, they show a slightly red-shifted absorption of about 50 to 100 nm. , Some organisms, such as certain species of cyanobacteria, have even evolved to adapt to low intensity light conditions rearranging their LHC structures to absorb infrared light by a well-established phenomenon known as far red light photoacclimation (FarLiP) in which paralagous subunits of PS-I and PS-II are expressed for the purpose of harvesting longer wavelengths in environments with low levels of white light, but even in these conditions, the maximum absorption is observed around 810 nm. , …”

Charge-transfer states in photosynthesis and organic solar cells

“…In another way, Stark spectroscopy is used to study the CT character of excited states (Romero et al, 2017). Alongside calculations based on time-dependent densityfunctional theory (TDDFT) go hand-in-hand with these techniques and can improve our understanding of spectra (Sirohiwal and Pantazis, 2022).…”

Understanding Primary Charge Separation in the Heliobacterial Reaction Center

“…By introducing a dielectric medium one can account for (additional) screening effects. MD calculations can be performed using force fields specifically reparametrized for photosynthetic pigments. , These methods can lead to further valuable insights. ,,,,,− …”