The Evolution and Evolvability of Photosystem II

• Published in: Annual review of plant biology Vol. 74; no. 1; pp. 225 - 257
• Main Authors: Oliver, Thomas, Kim, Tom D, Trinugroho, Joko P, Cordón-Preciado, Violeta, Wijayatilake, Nitara, Bhatia, Aaryan, Rutherford, A. William, Cardona, Tanai
• Format: Journal Article
• Language: English
• Published: United States Annual Reviews 22.05.2023; Annual Reviews, Inc
• Subjects: Catalysis; Cyanobacteria; Cyanobacteria - genetics; Cyanobacteria - metabolism; Environmental conditions; Enzymes; Evolution; origin of life; Oxidation; Oxidation-Reduction; Oxygen; Photochemistry; Photosynthesis; Photosynthesis - genetics; photosystem; Photosystem II; Photosystem II Protein Complex - genetics; Photosystem II Protein Complex - metabolism; Prokaryotes; Water; water oxidation; photosystem; origin of life; water oxidation; photosynthesis; D1; cyanobacteria
• ISSN: 1543-5008; 1545-2123
• DOI: 10.1146/annurev-arplant-070522-062509

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.