The Evolution and Evolvability of Photosystem II

Oliver, Thomas; Kim, Tom D.; Trinugroho, Joko P.; Cordón-Preciado, Violeta; Wijayatilake, Nitara; Bhatia, Aaryan; Rutherford, A. William; Cardona, Tanai

doi:10.1146/annurev-arplant-070522-062509

Cited by 52Photosynthetic Processes and MechanismsMetalloenzymes and iron-sulfur proteinsAdvanced Photocatalysis Techniques

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The Evolution and Evolvability of Photosystem II

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Oliver, Thomas, Kim, Tom D., Trinugroho, Joko P., Cordón-Preciado, Violeta, Wijayatilake, Nitara, Bhatia, Aaryan, Rutherford, A. William, Cardona, Tanai·2023·Annual Review of Plant Biology

DOI 10.1146/annurev-arplant-070522-062509

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Abstract

Photosystem II is the water-oxidizing and O 2-evolving enzyme of photosynthesis. How and when this remarkable enzyme arose are fundamental questions in the history of life that have remained difficult to answer. Here, recent advances in our understanding of the origin and evolution of photosystem II are reviewed and discussed in detail. The evolution of photosystem II indicates that water oxidation originated early in the history of life, long before the diversification of cyanobacteria and other major groups of prokaryotes, challenging and transforming current paradigms on the evolution of photosynthesis. We show that photosystem II has remained virtually unchanged for billions of years, and yet the nonstop duplication process of the D1 subunit of photosystem II, which controls photochemistry and catalysis, has enabled the enzyme to become adaptable to variable environmental conditions and even to innovate enzymatic functions beyond water oxidation. We suggest that this evolvability can be harnessed to develop novel light-powered enzymes with the capacity to carry out complex multistep oxidative transformations for sustainable biocatalysis.

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“Following the original development of photosynthesis, two versions of the original photosystem, called photosystem I and photosystem II, were coupled, enabling solar photons to split water (instead of hydrogen sulfide), producing molecular oxygen and hydrogen [142].”
From Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell (2024) · cites this paper as [142]

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“Following the original development of photosynthesis, two versions of the original photosystem, called photosystem I and photosystem II, were coupled, enabling solar photons to split water (instead of hydrogen sulfide), producing molecular oxygen and hydrogen [142].”
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Authors: Oliver, T., Kim, T. D., Trinugroho, J. P., Cordón-Preciado, V., Wijayatilake, N., Bhatia, A., Rutherford, A. W., & Cardona, T.
Affiliations: Imperial College London (GB)
Binus University (ID)
ORCID: Oliver, Thomas
Kim, Tom D.
Trinugroho, Joko P.
Cordón-Preciado, Violeta
Wijayatilake, Nitara
Bhatia, Aaryan
Rutherford, A. William
Cardona, Tanai
Venue: Annual Review of Plant Biology
Publisher: Annual Reviews
Published: 2023-05-22
Volume: 74
Issue: 1
Pages: 225-257
ISSN: 1543-5008 (ISSN-L)
1545-2123
DOI: 10.1146/annurev-arplant-070522-062509
OpenAlex: W4323537719
Cited by: 52
References: 161
Citations by year: 2026: 15 · 2025: 11 · 2024: 22 · 2023: 4
FWCI: 1.38
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: Annual Review of Plant Biology (publishedVersion, cc-by)
PubMed (publishedVersion)
VU Research Portal (publishedVersion, other-oa)
Spiral (Imperial College London) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders: UK Research and Innovation (MR/T017546/1)
Leverhulme Trust (RPG-2017-223)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Metalloenzymes and iron-sulfur proteins
Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Advanced Photocatalysis Techniques
Keywords: photosystem II, evolution of photosynthesis, water oxidation, origin of photosynthesis, evolvability, cyanobacteria, biocatalysis, oxidative transformation
MeSH terms: Cyanobacteria, Oxidation-Reduction, Oxygen, Photosynthesis, Water, Photosystem II Protein Complex

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The Evolution and Evolvability of Photosystem II

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