Nanophotonics of higher-plant photosynthetic membranes

Abstract

The thylakoid membrane inside chloroplasts hosts the light-dependent reactions of photosynthesis. Its embedded protein complexes are responsible for light harvesting, excitation energy transfer, charge separation, and transport. In higher plants, when the illumination conditions vary, the membrane adapts its composition and nanoscale morphology, which is characterized by appressed and non-appressed regions known as grana and stroma lamellae, respectively. Here we investigate the nanophotonic regime of light propagation in chloroplasts of higher plants and identify novel mechanisms in the optical response of the thylakoid membrane. Our results indicate that the relative contributions of light scattering and absorption to the overall optical response of grana strongly depend on the concentration of the light-harvesting complexes. For the pigment concentrations typically found in chloroplasts, the two mechanisms have comparable strengths, and their relative value can be tuned by variations in the protein composition or in the granal diameter. Furthermore, we find that collective modes in ensembles of grana significantly increase light absorption at selected wavelengths, even in the presence of moderate biological disorder. Small variations in the granal separation or a large disorder can dismantle this collective response. We propose that chloroplasts use this mechanism as a strategy against dangerously high illumination conditions, triggering a transition to low-absorbing states. We conclude that the morphological separation of the thylakoid membrane in higher plants supports strong nanophotonic effects, which may be used by chloroplasts to regulate light absorption. This adaptive self-organization capability is of interest as a model for novel bioinspired optical materials for artificial photosynthesis, imaging, and sensing.

Fig. 1

a Schematic of a higher-plant chloroplast showing the outer chloroplast membrane and the thylakoid membrane within. The thylakoid is morphologically separated into tightly stacked, discoidal grana, and unstacked stroma lamellae. The photosynthetically active wavelengths of the incident light are shown approximately to scale, corresponding closely to the sizes of grana while being two orders of magnitude larger than the embedded LHCs. b An individual granum schematized as a periodic stack of discoidal layers. c Each granal layer consists of four strata: two protein-embedding lipid bilayers (green), a lumen region (mid blue), and a thinner stroma region (light blue). d Schematic of an array of PSII-LHCII supercomplexes embedded in the lipid bilayer of the thylakoid membrane. e A picture of photosynthetic light harvesting in which the optical properties at each structural level provide an effective light environment for the next smaller level. Whereas the light distribution at higher levels (green) inhabits the ray optics regime, and excitation energy transfer within the protein complexes requires near-field quantum dynamical methods, the intermediate levels inside the chloroplast (red) demand a nanophotonic description

Fig. 2

a Extinction coefficient of the protein phase (black), the thylakoid stratum (red), and the granal layer (green) as a function of the chlorophyll molar concentration c_protein (with respect to the protein phase) at λ = 680 nm. The inset shows a representative absorption spectrum of LHCIIs. b Absorption (continuous lines) and scattering (dashed lines) efficiencies of cylindrical grana as a function of the extinction coefficient k of the granal layer. The granal height is H = 300 nm, and the diameter D is parametrized from 200 to 600 nm. c Absorption efficiency of cylindrical grana with D = 300 nm as a function of H, parametrized for k from 0.01 to 0.1. d Scattering efficiency of cylindrical grana with k = 0.01 as a function of H, parametrized for D from 200 nm to 600 nm. All calculations are at λ = 680 nm

Fig. 3. Spatial distributions of the light intensity in granal models of increasing complexity.

a Reference case of a homogeneous slab with a 300 nm height, infinite width, and k = 0.01. b A cylindrical homogeneous granum with H = 300 nm, D = 300 nm, and k = 0.01. c An ordered granum made of 20 discoidal layers, each consisting of four strata with thicknesses of t_thylakoid = 3 nm, t_lumen = 7.5 nm, and t_stroma = 1.8 nm (the total granal size is approximately the same as in b). d A granum made of laterally displaced discoidal layers 15.3 nm in thickness. Each layer is homogeneous with k = 0.01. The lateral displacements with respect to the x and y axes are sampled from Gaussian distributions with σ_layer = 40 nm. The incident light is a plane wave propagating along the z axis from above with λ = 680 nm that is linearly polarized along the x axis with unitary intensity

Fig. 4

a Absorption (left axis, green) and scattering (right axis, yellow) efficiencies for a granum with laterally displaced discoidal layers as a function of the standard deviation of the position σ_layer. The illumination source is a plane wave propagating parallel to the granal axis. b Absorption (left axis, continuous lines) and scattering (right axis, dashed lines) efficiencies as a function of the illumination angle θ of the plane wave for σ_layer = 10 nm (black), 35 nm (red), 60 nm (green), and 85 nm (blue). For each σ_layer and θ, the efficiencies are calculated as the average of ten different realizations of grana. All data are for D = H = 300 nm, k = 0.01 (c_protein = 60 mol L⁻¹), and λ = 680 nm

Fig. 5. Upper row: an infinite ensemble of grana.

a Absorption (mapped as color on a logarithmic scale) as a function of S and λ for H = 200 nm, AF = 20%, and k = 0.01. The inset shows spectra for S = 575, 578, and 583 nm and the spectrum of a slab with a dotted line. Spatial distribution of the light intensity in the plane at half-height for b S = 578 nm and c S = 583 nm. Bottom row: a finite ensemble of grana with H = 200 nm. d Schematic with a central granum and surrounding rings. e Absorption spectra (continuous lines) for ensembles with S = 578 nm and an increasing number of rings N, from 1–7. f Absorption spectra for ensembles with N = 7, S = 557 nm, and a constant extinction coefficient k = 0.01 (solid line), or k with spectral dispersion (dashed line)

Fig. 6

a Absorption spectra of ensembles of grana for different realizations of disorder with increasing standard deviation σ_granum of the positions of the grana (the spectrum of the ordered ensemble is shown with a black line) from 0 to 50 nm. b Light intensity distribution on the surfaces of the grana. c Absorption spectra of an ensemble of grana for three realizations of disorder in the position of the discoidal layers with σ_layer = 30 nm (red) and 50 nm (green). The black line shows the ordered ensemble with σ_layer = 0 nm. d Light intensity distribution on the surfaces of the granal layers