Impact of energy limitations on function and resilience in long-wavelength photosystem II
- Imperial College London, United Kingdom
- Consiglio Nazionale delle Ricerche, Italy
- Freie Universität Berlin, Germany
- Institut de Biologie Physico-Chimique, France
- CEA Saclay, France
Abstract
Photosystem II (PSII) uses the energy from red light to split water and reduce quinone, an energy-demanding process based on chlorophyll a (Chl-a) photochemistry. Two types of cyanobacterial PSII can use chlorophyll d (Chl-d) and chlorophyll f (Chl-f) to perform the same reactions using lower energy, far-red light. PSII from Acaryochloris marina has Chl-d replacing all but one of its 35 Chl-a, while PSII from Chroococcidiopsis thermalis, a facultative far-red species, has just 4 Chl-f and 1 Chl-d and 30 Chl-a. From bioenergetic considerations, the far-red PSII were predicted to lose photochemical efficiency and/or resilience to photodamage. Here, we compare enzyme turnover efficiency, forward electron transfer, back-reactions and photodamage in Chl-f-PSII, Chl-d-PSII and Chl-a-PSII. We show that: i) all types of PSII have a comparable efficiency in enzyme turnover; ii) the modified energy gaps on the acceptor side of Chl-d-PSII favour recombination via PD1+Phe- repopulation, leading to increased singlet oxygen production and greater sensitivity to high-light damage compared to Chl-a-PSII and Chl-f-PSII; iii) the acceptor-side energy gaps in Chl-f-PSII are tuned to avoid harmful back reactions, favouring resilience to photodamage over efficiency of light usage. The results are explained by the differences in the redox tuning of the electron transfer cofactors Phe and QA and in the number and layout of the chlorophylls that share the excitation energy with the primary electron donor. PSII has adapted to lower energy in two distinct ways, each appropriate for its specific environment but with different functional penalties.
Data availability
Data and materials availability: All data generated and analysed during this study have been included in the manuscript and supporting file and provided as Source Data files.
Article and author information
Author details
A William Rutherford
Funding
Biotechnology and Biological Sciences Research Council (BB/R001383/1)
- Stefania Viola
- William Roseby
- Andrea Fantuzzi
- A William Rutherford
Biotechnology and Biological Sciences Research Council (BB/V002015/1)
- Stefania Viola
- William Roseby
- Andrea Fantuzzi
- A William Rutherford
Biotechnology and Biological Sciences Research Council (BB/R00921X)
- Stefania Viola
- William Roseby
- Andrea Fantuzzi
- A William Rutherford
Labex (ANR-11-LABX-0011-01)
- Julien Sellés
French Infrastructure for Integrated Structural Biology (ANR-10-INBS-05)
- Alain Boussac
Fondazione Cariplo (2016-0667)
- Stefano Santabarbara
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- David M Kramer, Michigan State University, United States
Version history
- Preprint posted: April 6, 2022 (view preprint)
- Received: April 30, 2022
- Accepted: July 18, 2022
- Accepted Manuscript published: July 19, 2022 (version 1)
- Version of Record published: September 2, 2022 (version 2)
- Version of Record updated: January 5, 2023 (version 3)
Copyright
© 2022, Viola et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Impact of energy limitations on function and resilience in long-wavelength photosystem II
eLife 11:e79890.
https://doi.org/10.7554/eLife.79890
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