Cargando…
Atomic Force Microscopy Visualizes Mobility of Photosynthetic Proteins in Grana Thylakoid Membranes
Thylakoid membranes in chloroplasts contain photosynthetic protein complexes that convert light energy into chemical energy. Photosynthetic protein complexes are considered to undergo structural reorganization to maintain the efficiency of photochemical reactions. A detailed description of the mobil...
Autores principales: | , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The Biophysical Society
2020
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7175462/ https://www.ncbi.nlm.nih.gov/pubmed/32224302 http://dx.doi.org/10.1016/j.bpj.2020.02.029 |
_version_ | 1783524837077024768 |
---|---|
author | Onoa, Bibiana Fukuda, Shingo Iwai, Masakazu Bustamante, Carlos Niyogi, Krishna K. |
author_facet | Onoa, Bibiana Fukuda, Shingo Iwai, Masakazu Bustamante, Carlos Niyogi, Krishna K. |
author_sort | Onoa, Bibiana |
collection | PubMed |
description | Thylakoid membranes in chloroplasts contain photosynthetic protein complexes that convert light energy into chemical energy. Photosynthetic protein complexes are considered to undergo structural reorganization to maintain the efficiency of photochemical reactions. A detailed description of the mobility of photosynthetic complexes in real time is necessary to understand how macromolecular organization of the membrane is altered by environmental fluctuations. Here, we used high-speed atomic force microscopy to visualize and characterize the in situ mobility of individual protein complexes in grana thylakoid membranes isolated from Spinacia oleracea. Our observations reveal that these membranes can harbor complexes with at least two distinctive classes of mobility. A large fraction of grana membranes contained proteins with quasistatic mobility exhibiting molecular displacements smaller than 10 nm(2). In the remaining fraction, the protein mobility is variable with molecular displacements of up to 100 nm(2). This visualization at high spatiotemporal resolution enabled us to estimate an average diffusion coefficient of ∼1 nm(2) s(−1). Interestingly, both confined and Brownian diffusion models could describe the protein mobility of the second group of membranes. We also provide the first direct evidence, to our knowledge, of rotational diffusion of photosynthetic complexes. The rotational diffusion of photosynthetic complexes could be an adaptive response to the high protein density in the membrane to guarantee the efficiency of electron transfer reactions. This characterization of the mobility of individual photosynthetic complexes in grana membranes establishes a foundation that could be adapted to study the dynamics of the complexes inside intact and photosynthetically functional thylakoid membranes to be able to understand its structural responses to diverse environmental fluctuations. |
format | Online Article Text |
id | pubmed-7175462 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | The Biophysical Society |
record_format | MEDLINE/PubMed |
spelling | pubmed-71754622020-10-10 Atomic Force Microscopy Visualizes Mobility of Photosynthetic Proteins in Grana Thylakoid Membranes Onoa, Bibiana Fukuda, Shingo Iwai, Masakazu Bustamante, Carlos Niyogi, Krishna K. Biophys J Article Thylakoid membranes in chloroplasts contain photosynthetic protein complexes that convert light energy into chemical energy. Photosynthetic protein complexes are considered to undergo structural reorganization to maintain the efficiency of photochemical reactions. A detailed description of the mobility of photosynthetic complexes in real time is necessary to understand how macromolecular organization of the membrane is altered by environmental fluctuations. Here, we used high-speed atomic force microscopy to visualize and characterize the in situ mobility of individual protein complexes in grana thylakoid membranes isolated from Spinacia oleracea. Our observations reveal that these membranes can harbor complexes with at least two distinctive classes of mobility. A large fraction of grana membranes contained proteins with quasistatic mobility exhibiting molecular displacements smaller than 10 nm(2). In the remaining fraction, the protein mobility is variable with molecular displacements of up to 100 nm(2). This visualization at high spatiotemporal resolution enabled us to estimate an average diffusion coefficient of ∼1 nm(2) s(−1). Interestingly, both confined and Brownian diffusion models could describe the protein mobility of the second group of membranes. We also provide the first direct evidence, to our knowledge, of rotational diffusion of photosynthetic complexes. The rotational diffusion of photosynthetic complexes could be an adaptive response to the high protein density in the membrane to guarantee the efficiency of electron transfer reactions. This characterization of the mobility of individual photosynthetic complexes in grana membranes establishes a foundation that could be adapted to study the dynamics of the complexes inside intact and photosynthetically functional thylakoid membranes to be able to understand its structural responses to diverse environmental fluctuations. The Biophysical Society 2020-04-21 2020-03-13 /pmc/articles/PMC7175462/ /pubmed/32224302 http://dx.doi.org/10.1016/j.bpj.2020.02.029 Text en © 2020 Biophysical Society. http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
spellingShingle | Article Onoa, Bibiana Fukuda, Shingo Iwai, Masakazu Bustamante, Carlos Niyogi, Krishna K. Atomic Force Microscopy Visualizes Mobility of Photosynthetic Proteins in Grana Thylakoid Membranes |
title | Atomic Force Microscopy Visualizes Mobility of Photosynthetic Proteins in Grana Thylakoid Membranes |
title_full | Atomic Force Microscopy Visualizes Mobility of Photosynthetic Proteins in Grana Thylakoid Membranes |
title_fullStr | Atomic Force Microscopy Visualizes Mobility of Photosynthetic Proteins in Grana Thylakoid Membranes |
title_full_unstemmed | Atomic Force Microscopy Visualizes Mobility of Photosynthetic Proteins in Grana Thylakoid Membranes |
title_short | Atomic Force Microscopy Visualizes Mobility of Photosynthetic Proteins in Grana Thylakoid Membranes |
title_sort | atomic force microscopy visualizes mobility of photosynthetic proteins in grana thylakoid membranes |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7175462/ https://www.ncbi.nlm.nih.gov/pubmed/32224302 http://dx.doi.org/10.1016/j.bpj.2020.02.029 |
work_keys_str_mv | AT onoabibiana atomicforcemicroscopyvisualizesmobilityofphotosyntheticproteinsingranathylakoidmembranes AT fukudashingo atomicforcemicroscopyvisualizesmobilityofphotosyntheticproteinsingranathylakoidmembranes AT iwaimasakazu atomicforcemicroscopyvisualizesmobilityofphotosyntheticproteinsingranathylakoidmembranes AT bustamantecarlos atomicforcemicroscopyvisualizesmobilityofphotosyntheticproteinsingranathylakoidmembranes AT niyogikrishnak atomicforcemicroscopyvisualizesmobilityofphotosyntheticproteinsingranathylakoidmembranes |