Title: Energetic robustness to large scale structural fluctuations in a photosynthetic supercomplex

Journal Article · · Nature Communications

Abstract Photosynthetic organisms transport and convert solar energy with near-unity quantum efficiency using large protein supercomplexes held in flexible membranes. The individual proteins position chlorophylls to tight tolerances considered critical for fast and efficient energy transfer. The variability in protein organization within the supercomplexes, and how efficiency is maintained despite variability, had been unresolved. Here, we report on structural heterogeneity in the 2-MDa cyanobacterial PSI-IsiA photosynthetic supercomplex observed using Cryo-EM, revealing large-scale variances in the positions of IsiA relative to PSI. Single-molecule measurements found efficient IsiA-to-PSI energy transfer across all conformations, along with signatures of transiently decoupled IsiA. Structure based calculations showed that rapid IsiA-to-PSI energy transfer is always maintained, and even increases by three-fold in rare conformations via IsiA-specific chls. We postulate that antennae design mitigates structural fluctuations, providing a mechanism for robust energy transfer in the flexible membrane.

Research Organization:
Arizona State Univ., Tempe, AZ (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Sponsoring Organization:
National Science Foundation (NSF); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)
Grant/Contract Number:
SC0018097; SC0022956
OSTI ID:
1993523
Journal Information:
Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 14; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (69)

UCSF Chimera?A visualization system for exploratory research and analysis journal January 2004
UCSF ChimeraX: Meeting modern challenges in visualization and analysis: UCSF ChimeraX Visualization System journal September 2017
Multi-body Refinement of Cryo-EM Images in RELION book December 2020
Origin and early evolution of photosynthesis journal August 1992
Function, regulation and distribution of IsiA, a membrane-bound chlorophyll a-antenna protein in cyanobacteria journal January 2018
Function of the IsiA pigment–protein complex in vivo journal March 2019
Excitation-energy quenching in aggregates of the LHC II chlorophyll-protein complex: a time-resolved fluorescence study journal February 1993
Energy transfer and trapping in photosynthesis journal August 1994
Excitation energy transfer, trapping and annihilation in photosynthetic systems journal June 1985
Spectroscopic properties of PSI–IsiA supercomplexes from the cyanobacterium Synechococcus PCC 7942 journal December 2002
Time-Resolved Fluorescence Emission Measurements of Photosystem I Particles of Various Cyanobacteria: A Unified Compartmental Model journal July 2001
The Flow of Excitation Energy in LHCII Monomers: Implications for the Structural Model of the Major Plant Antenna journal December 1998
Femtosecond spectroscopy of photosynthetic light-harvesting systems journal October 1997
Energy transfer and trapping in the Photosystem I complex of Synechococcus PCC 7942 and in its supercomplex with IsiA journal June 2004
Fluorescence quenching of IsiA in early stage of iron deficiency and at cryogenic temperatures journal December 2007
The photoprotective molecular switch in the photosystem II antenna journal January 2012
PSI–LHCI of Chlamydomonas reinhardtii : Increasing the absorption cross section without losing efficiency journal April 2015
Reevaluating the mechanism of excitation energy regulation in iron-starved cyanobacteria journal March 2017
Multiple LHCII antennae can transfer energy efficiently to a single Photosystem I journal May 2017
The amazing phycobilisome journal April 2020
A Mechanism of Energy Dissipation in Cyanobacteria journal March 2009
Membrane-dependent heterogeneity of LHCII characterized using single-molecule spectroscopy journal August 2021
Structure and functional role of supercomplexes of IsiA and Photosystem I in cyanobacterial photosynthesis journal April 2005
CTFFIND4: Fast and accurate defocus estimation from electron micrographs journal November 2015
Gctf: Real-time CTF determination and correction journal January 2016
Dynamic Changes of IsiA-Containing Complexes during Long-Term Iron Deficiency in Synechocystis sp. PCC 6803 journal January 2017
SerialEM: A Program for Automated Tilt Series Acquisition on Tecnai Microscopes Using Prediction of Specimen Position journal July 2003
Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms journal March 2016
Ultrafast Excitation Energy Dynamics in a Diatom Photosystem I-Antenna Complex: A Femtosecond Fluorescence Upconversion Study journal February 2019
LHCII Populations in Different Quenching States Are Present in the Thylakoid Membranes in a Ratio that Depends on the Light Conditions journal June 2015
Photosynthetic Light-Harvesting Pigment−Protein Complexes:  Toward Understanding How and Why journal January 1996
Time-Resolved Absorption and Emission Show that the CP43‘ Antenna Ring of Iron-Stressed Synechocystis sp. PCC6803 Is Efficiently Coupled to the Photosystem I Reaction Center Core , journal April 2003
Supramolecular Organization and Dual Function of the IsiA Chlorophyll-Binding Protein in Cyanobacteria journal August 2004
Aggregates of the Chlorophyll-Binding Protein IsiA (CP43‘) Dissipate Energy in Cyanobacteria journal August 2005
A Novel Photosynthetic Strategy for Adaptation to Low-Iron Aquatic Environments journal February 2011
Protein–Protein Interactions Induce pH-Dependent and Zeaxanthin-Independent Photoprotection in the Plant Light-Harvesting Complex, LHCII journal October 2021
Ultrafast Energy Transfer Involving the Red Chlorophylls of Cyanobacterial Photosystem I Probed through Two-Dimensional Electronic Spectroscopy journal August 2018
Superradiance and Exciton (De)localization in Light-Harvesting Complex II from Green Plants? journal June 2002
Detection of Intensity Change Points in Time-Resolved Single-Molecule Measurements journal January 2005
Spectroscopic Study of the CP43′ Complex and the PSI–CP43′ Supercomplex of the Cyanobacterium Synechocystis PCC 6803 journal November 2011
Pigment Organization and Transfer of Electronic Excitation in the Photosynthetic Unit of Purple Bacteria journal May 1997
Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria journal August 2001
A giant chlorophyll–protein complex induced by iron deficiency in cyanobacteria journal August 2001
Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection journal July 2017
Natural strategies for photosynthetic light harvesting journal June 2014
Quantifying the local resolution of cryo-EM density maps journal November 2013
MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy journal February 2017
Structure of the plant photosystem I supercomplex at 2.6 Å resolution journal March 2017
U1 snRNP regulates cancer cell migration and invasion in vitro journal January 2020
Effects of cryo-EM cooling on structural ensembles journal March 2022
Structural basis for energy and electron transfer of the photosystem I–IsiA–flavodoxin supercomplex journal February 2020
Structural variability, coordination and adaptation of a native photosynthetic machinery journal July 2020
Positive-unlabeled convolutional neural networks for particle picking in cryo-electron micrographs journal October 2019
The structure of the stress-induced photosystem I–IsiA antenna supercomplex journal May 2019
Structure of a cyanobacterial photosystem I surrounded by octadecameric IsiA antenna proteins journal May 2020
Single-molecule spectroscopy reveals photosynthetic LH2 complexes switch between emissive states journal June 2013
Mobility of the IsiA Chlorophyll-binding Protein in Cyanobacterial Thylakoid Membranes journal June 2004
Thylakoid Membrane Architecture in Synechocystis Depends on CurT, a Homolog of the Granal CURVATURE THYLAKOID1 Proteins journal August 2016
Coot model-building tools for molecular graphics journal November 2004
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
Estimation of high-order aberrations and anisotropic magnification from cryo-EM data sets in RELION -3.1 journal February 2020
Real-space refinement in PHENIX for cryo-EM and crystallography journal May 2018
Adaptation of the photosynthetic electron transport chain in cyanobacteria to iron deficiency: The function of IdiA and IsiA journal January 2004
A Novel Mode of Photoprotection Mediated by a Cysteine Residue in the Chlorophyll Protein IsiA journal February 2021
Structure and Energy Transfer in Photosystems of Oxygenic Photosynthesis journal June 2015
From isolated light-harvesting complexes to the thylakoid membrane: a single-molecule perspective journal January 2018
Ein Beitrag zur Theorie der Photosynthese journal June 1947
Characterisation of molecular motions in cryo-EM single-particle data by multi-body refinement in RELION journal June 2018
Identification of distinct pH- and zeaxanthin-dependent quenching in LHCSR3 from Chlamydomonas reinhardtii journal January 2021