Elucidating interprotein energy transfer dynamics within the antenna network from purple bacteria.

cryogenic electron microscopy light harvesting photosynthesis purple bacteria ultrafast spectroscopy

Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
11 07 2023
Historique:
pmc-release: 03 01 2024
medline: 5 7 2023
pubmed: 3 7 2023
entrez: 3 7 2023
Statut: ppublish

Résumé

In photosynthesis, absorbed light energy transfers through a network of antenna proteins with near-unity quantum efficiency to reach the reaction center, which initiates the downstream biochemical reactions. While the energy transfer dynamics within individual antenna proteins have been extensively studied over the past decades, the dynamics between the proteins are poorly understood due to the heterogeneous organization of the network. Previously reported timescales averaged over such heterogeneity, obscuring individual interprotein energy transfer steps. Here, we isolated and interrogated interprotein energy transfer by embedding two variants of the primary antenna protein from purple bacteria, light-harvesting complex 2 (LH2), together into a near-native membrane disc, known as a nanodisc. We integrated ultrafast transient absorption spectroscopy, quantum dynamics simulations, and cryogenic electron microscopy to determine interprotein energy transfer timescales. By varying the diameter of the nanodiscs, we replicated a range of distances between the proteins. The closest distance possible between neighboring LH2, which is the most common in native membranes, is 25 Å and resulted in a timescale of 5.7 ps. Larger distances of 28 to 31 Å resulted in timescales of 10 to 14 ps. Corresponding simulations showed that the fast energy transfer steps between closely spaced LH2 increase transport distances by ∼15%. Overall, our results introduce a framework for well-controlled studies of interprotein energy transfer dynamics and suggest that protein pairs serve as the primary pathway for the efficient transport of solar energy.

Identifiants

pubmed: 37399405
doi: 10.1073/pnas.2220477120
pmc: PMC10334754
doi:

Substances chimiques

Light-Harvesting Protein Complexes 0

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2220477120

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Auteurs

Dihao Wang (D)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

Olivia C Fiebig (OC)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

Dvir Harris (D)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

Hila Toporik (H)

School of Molecular Sciences, Arizona State University, Tempe, AZ 85281.
Biodesign Center for Applied Structural Discovery, Arizona State University, Tempe, AZ 85281.

Yi Ji (Y)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

Chern Chuang (C)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

Muath Nairat (M)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

Ashley L Tong (AL)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

John I Ogren (JI)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

Stephanie M Hart (SM)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

Jianshu Cao (J)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

James N Sturgis (JN)

LISM UMR 7255, CNRS and Aix-Marseille University, Marseille Cedex 9 13402, France.

Yuval Mazor (Y)

School of Molecular Sciences, Arizona State University, Tempe, AZ 85281.
Biodesign Center for Applied Structural Discovery, Arizona State University, Tempe, AZ 85281.

Gabriela S Schlau-Cohen (GS)

Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139.

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Classifications MeSH