Structure of the light harvesting 2 complex reveals two carotenoid energy transfer pathways in a photosynthetic bacterium

AbstractWe report the 2.4 Å resolution structure of the light harvesting 2 complex (LH2) from Marichromatium (Mch.) purpuratum determined by electron cryo-microscopy. The structure contains a heptameric ring that is unique among all known LH2 structures, explaining the unusual spectroscopic properties of this bacterial antenna complex. Two sets of distinct carotenoids are identified in the structure, and a network of energy transfer pathways from the carotenoids to bacteriochlorophyll a molecules is shown. The geometry imposed by the heptameric ring controls the resonant coupling of the long wavelength energy absorption band. Together, these details reveal key aspects of the assembly and oligomeric form of purple bacterial LH2 complexes that were previously inaccessible by any technique.One Sentence SummaryThe structure of a heptameric LH2 antenna complex reveals new energy transfer pathways and the basis for assembling LH rings.

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The 2.4 Å cryo-EM structure of a heptameric light-harvesting 2 complex reveals two carotenoid energy transfer pathways

Science Advances ◽

10.1126/sciadv.abe4650 ◽

2021 ◽

Vol 7 (7) ◽

pp. eabe4650 ◽

Cited By ~ 1

Author(s):

Alastair T. Gardiner ◽

Katerina Naydenova ◽

Pablo Castro-Hartmann ◽

Tu C. Nguyen-Phan ◽

Christopher J. Russo ◽

...

Keyword(s):

Electron Microscopy ◽

Energy Transfer ◽

Light Harvesting ◽

Spectroscopic Properties ◽

Resonant Coupling ◽

Long Wavelength ◽

Antenna Complex ◽

Oligomeric Form ◽

Key Aspects ◽

Resolution Structure

We report the 2.4 Ångström resolution structure of the light-harvesting 2 (LH2) complex from Marichromatium (Mch.) purpuratum determined by cryogenic electron microscopy. The structure contains a heptameric ring that is unique among all known LH2 structures, explaining the unusual spectroscopic properties of this bacterial antenna complex. We identify two sets of distinct carotenoids in the structure and describe a network of energy transfer pathways from the carotenoids to bacteriochlorophyll a molecules. The geometry imposed by the heptameric ring controls the resonant coupling of the long-wavelength energy absorption band. Together, these details reveal key aspects of the assembly and oligomeric form of purple bacterial LH2 complexes that were previously inaccessible by any technique.

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A photosynthetic antenna complex foregoes unity carotenoid-to-bacteriochlorophyll energy transfer efficiency to ensure photoprotection

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1920923117 ◽

2020 ◽

Vol 117 (12) ◽

pp. 6502-6508 ◽

Cited By ~ 1

Author(s):

Dariusz M. Niedzwiedzki ◽

David J. K. Swainsbury ◽

Daniel P. Canniffe ◽

C. Neil Hunter ◽

Andrew Hitchcock

Keyword(s):

Energy Transfer ◽

Transient Absorption ◽

Light Harvesting ◽

Protein Complexes ◽

Fluorescence Emission ◽

Energy Transfer Efficiency ◽

Transfer Efficiency ◽

Light Harvesting Complexes ◽

Antenna Complex ◽

Pigment Protein Complexes

Carotenoids play a number of important roles in photosynthesis, primarily providing light-harvesting and photoprotective energy dissipation functions within pigment–protein complexes. The carbon–carbon double bond (C=C) conjugation length of carotenoids (N), generally between 9 and 15, determines the carotenoid-to-(bacterio)chlorophyll [(B)Chl] energy transfer efficiency. Here we purified and spectroscopically characterized light-harvesting complex 2 (LH2) fromRhodobacter sphaeroidescontaining theN= 7 carotenoid zeta (ζ)-carotene, not previously incorporated within a natural antenna complex. Transient absorption and time-resolved fluorescence show that, relative to the lifetime of the S1state of ζ-carotene in solvent, the lifetime decreases ∼250-fold when ζ-carotene is incorporated within LH2, due to transfer of excitation energy to the B800 and B850 BChlsa. These measurements show that energy transfer proceeds with an efficiency of ∼100%, primarily via the S1→ Qxroute because the S1→ S0fluorescence emission of ζ-carotene overlaps almost perfectly with the Qxabsorption band of the BChls. However, transient absorption measurements performed on microsecond timescales reveal that, unlike the nativeN≥ 9 carotenoids normally utilized in light-harvesting complexes, ζ-carotene does not quench excited triplet states of BChla, likely due to elevation of the ζ-carotene triplet energy state above that of BChla. These findings provide insights into the coevolution of photosynthetic pigments and pigment–protein complexes. We propose that theN≥ 9 carotenoids found in light-harvesting antenna complexes represent a vital compromise that retains an acceptable level of energy transfer from carotenoids to (B)Chls while allowing acquisition of a new, essential function, namely, photoprotective quenching of harmful (B)Chl triplets.

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