Nanophotonics of higher-plant photosynthetic membranes

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

Research output: Contribution to JournalArticleAcademicpeer-review

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.

Original languageEnglish
Article number5
JournalLight: Science and Applications
Volume8
Issue number1
DOIs
Publication statusPublished - 1 Dec 2019

Fingerprint

Photosynthetic membranes
chloroplasts
Nanophotonics
Light absorption
membranes
Membranes
electromagnetic absorption
Photosynthesis
photosynthesis
Light-Harvesting Protein Complexes
Lighting
Proteins
Light propagation
illumination
Optical materials
Excitation energy
disorders
proteins
Chemical analysis
Pigments

Cite this

Capretti, A., Ringsmuth, A. K., van Velzen, J. F., Rosnik, A., Croce, R., & Gregorkiewicz, T. (2019). Nanophotonics of higher-plant photosynthetic membranes. Light: Science and Applications, 8(1), [5]. https://doi.org/10.1038/s41377-018-0116-8
Capretti, A. ; Ringsmuth, A. K. ; van Velzen, J. F. ; Rosnik, A. ; Croce, R. ; Gregorkiewicz, T. / Nanophotonics of higher-plant photosynthetic membranes. In: Light: Science and Applications. 2019 ; Vol. 8, No. 1.
@article{ee0255c3807d4d2bb103a1d906da8119,
title = "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.",
author = "A. Capretti and Ringsmuth, {A. K.} and {van Velzen}, {J. F.} and A. Rosnik and R. Croce and T. Gregorkiewicz",
year = "2019",
month = "12",
day = "1",
doi = "10.1038/s41377-018-0116-8",
language = "English",
volume = "8",
journal = "Light: Science & Applications",
issn = "2047-7538",
publisher = "Nature Publishing Group",
number = "1",

}

Capretti, A, Ringsmuth, AK, van Velzen, JF, Rosnik, A, Croce, R & Gregorkiewicz, T 2019, 'Nanophotonics of higher-plant photosynthetic membranes' Light: Science and Applications, vol. 8, no. 1, 5. https://doi.org/10.1038/s41377-018-0116-8

Nanophotonics of higher-plant photosynthetic membranes. / Capretti, A.; Ringsmuth, A. K.; van Velzen, J. F.; Rosnik, A.; Croce, R.; Gregorkiewicz, T.

In: Light: Science and Applications, Vol. 8, No. 1, 5, 01.12.2019.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - Nanophotonics of higher-plant photosynthetic membranes

AU - Capretti, A.

AU - Ringsmuth, A. K.

AU - van Velzen, J. F.

AU - Rosnik, A.

AU - Croce, R.

AU - Gregorkiewicz, T.

PY - 2019/12/1

Y1 - 2019/12/1

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85059761045&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85059761045&partnerID=8YFLogxK

U2 - 10.1038/s41377-018-0116-8

DO - 10.1038/s41377-018-0116-8

M3 - Article

VL - 8

JO - Light: Science & Applications

JF - Light: Science & Applications

SN - 2047-7538

IS - 1

M1 - 5

ER -

Capretti A, Ringsmuth AK, van Velzen JF, Rosnik A, Croce R, Gregorkiewicz T. Nanophotonics of higher-plant photosynthetic membranes. Light: Science and Applications. 2019 Dec 1;8(1). 5. https://doi.org/10.1038/s41377-018-0116-8