Nanophotonics of higher-plant photosynthetic membranes

A Capretti,J F Van Velzen,R Croce,A Rosnik,A K Ringsmuth,T Gregorkiewicz

doi:10.1038/s41377-018-0116-8

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.

Highlights

Photosynthesis, the conversion of sunlight into chemical energy, holds much promise for sustainable food and fuel production[1]
Preliminaries We model a granum as a stack of discoidal layers, with each made of four strata, as shown in Fig. 1b, c: the two strata of the thylakoid membrane, the lumen, and the stroma
Our results indicate that the ultrastructure of the thylakoid membrane in higher plants facilitates absorption regulation mechanisms based on nanophotonic geometric effects, which dominate at that scale

Summary

Introduction

Photosynthesis, the conversion of sunlight into chemical energy, holds much promise for sustainable food and fuel production[1]. The light-dependent reactions of photosynthesis occur at the level of the thylakoid membrane inside chloroplasts. The thylakoid membrane of plants is morphologically separated into tightly stacked grana and non-appressed stroma lamellae connecting the grana (Fig. 1a, b)[2]. The grana are discoidal in shape, with diameters typically reported in the range from 200 to 600 nm[2,3]. The thylakoid membrane separates the chloroplast into two fluid spaces, known as the stroma and lumen (Fig. 1c). There are well-known photochemical benefits of this morphology[4,5], the reasons for its evolution in higher plants remain only partially understood

Methods

Results

Conclusion