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
Publication 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.
Metrics
-
- 1,054
- Page views
-
- 379
- Downloads
-
- 3
- Citations
Article citation count generated by polling the highest count across the following sources: PubMed Central, Crossref, Scopus.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Impact of energy limitations on function and resilience in long-wavelength photosystem II
eLife 11:e79890.
https://doi.org/10.7554/eLife.79890
Further reading
-
- Structural Biology and Molecular Biophysics
- Cell Biology
Voltage-gated ion channels (VGICs) orchestrate electrical activities that drive mechanical functions in contractile tissues such as the heart and gut. In turn, contractions change membrane tension and impact ion channels. VGICs are mechanosensitive, but the mechanisms of mechanosensitivity remain poorly understood. Here, we leverage the relative simplicity of NaChBac, a prokaryotic voltage-gated sodium channel from Bacillus halodurans, to investigate mechanosensitivity. In whole-cell experiments on heterologously transfected HEK293 cells, shear stress reversibly altered the kinetic properties of NaChBac and increased its maximum current, comparably to the mechanosensitive eukaryotic sodium channel NaV1.5. In single-channel experiments, patch suction reversibly increased the open probability of a NaChBac mutant with inactivation removed. A simple kinetic mechanism featuring a mechanosensitive pore opening transition explained the overall response to force, whereas an alternative model with mechanosensitive voltage sensor activation diverged from the data. Structural analysis of NaChBac identified a large displacement of the hinged intracellular gate, and mutagenesis near the hinge diminished NaChBac mechanosensitivity, further supporting the proposed mechanism. Our results suggest that NaChBac is overall mechanosensitive due to the mechanosensitivity of a voltage-insensitive gating step associated with the pore opening. This mechanism may apply to eukaryotic VGICs, including NaV1.5.
-
- Structural Biology and Molecular Biophysics
The mono-ubiquitination of the histone protein H2B (H2Bub1) is a highly conserved histone post-translational modification that plays critical roles in many fundamental processes. In yeast, this modification is catalyzed by the conserved Bre1–Rad6 complex. Bre1 contains a unique N-terminal Rad6-binding domain (RBD), how it interacts with Rad6 and contributes to the H2Bub1 catalysis is unclear. Here, we present crystal structure of the Bre1 RBD–Rad6 complex and structure-guided functional studies. Our structure provides a detailed picture of the interaction between the dimeric Bre1 RBD and a single Rad6 molecule. We further found that the interaction stimulates Rad6’s enzymatic activity by allosterically increasing its active site accessibility and likely contribute to the H2Bub1 catalysis through additional mechanisms. In line with these important functions, we found that the interaction is crucial for multiple H2Bub1-regulated processes. Our study provides molecular insights into the H2Bub1 catalysis.
