Biochimica et Biophysica Acta (BBA) - Bioenergetics
Volume 1862, Issue 6, 1 June 2021, 148400
Time-resolved comparative molecular evolution of oxygenic photosynthesis
Thomas Oliver a, PatriciaSánchez-Baracaldo b, Anthony W.Larkum c, A. WilliamRutherford a, Tanai Cardona a
a Department of Life Sciences, Imperial College London, London, UK
b School of Geographical Sciences, University of Bristol, Bristol, UK
c University of Technology Sydney, Ultimo, NSW, Australia
Received 8 July 2020, Revised 1 February 2021, Accepted 12 February 2021, Available online 19 February 2021.
Colonies of cyanobacteria under the microscope. Credit: Ye.Maltsev/Shutterstock
Highlights
• The origin of oxygenic photosynthesis cannot be located on a species tree.
• Vampirovibrionia, Sericytochromatia and Margulisbacteria lost photosynthesis.
• Photosystem II can be as old as the oldest enzymes.
• Earliest type II reaction centres were structurally like water-splitting Photosystem II.
• Anoxygenic photosynthesis is not more primitive than oxygenic photosynthesis.
Abstract
Oxygenic photosynthesis starts with the oxidation of water to O2, a light-driven reaction catalysed by photosystem II. Cyanobacteria are the only prokaryotes capable of water oxidation and therefore, it is assumed that the origin of oxygenic photosynthesis is a late innovation relative to the origin of life and bioenergetics. However, when exactly water oxidation originated remains an unanswered question. Here we use phylogenetic analysis to study a gene duplication event that is unique to photosystem II: the duplication that led to the evolution of the core antenna subunits CP43 and CP47. We compare the changes in the rates of evolution of this duplication with those of some of the oldest well-described events in the history of life: namely, the duplication leading to the Alpha and Beta subunits of the catalytic head of ATP synthase, and the divergence of archaeal and bacterial RNA polymerases and ribosomes. We also compare it with more recent events such as the duplication of Cyanobacteria-specific FtsH metalloprotease subunits and the radiation leading to Margulisbacteria, Sericytochromatia, Vampirovibrionia, and other clades containing anoxygenic phototrophs. We demonstrate that the ancestral core duplication of photosystem II exhibits patterns in the rates of protein evolution through geological time that are nearly identical to those of the ATP synthase, RNA polymerase, or the ribosome. Furthermore, we use ancestral sequence reconstruction in combination with comparative structural biology of photosystem subunits, to provide additional evidence supporting the premise that water oxidation had originated before the ancestral core duplications. Our work suggests that photosynthetic water oxidation originated closer to the origin of life and bioenergetics than can be documented based on phylogenetic or phylogenomic species trees alone.
Abbreviations
MRCA most recent common ancestor LUCA the last universal common ancestor or the most recent common ancestor of life MSV Margulis bacteria, Sericytochromatia and Vampirovibrionia PSII photosystem IIPSI photosystem ICBP chlorophyll-binding protein RC reaction centre ROS reactive oxygen species GOE Great Oxidation Eventd D0 duplication leading to the origin of D1 and D2 subunits of photosystem IIdCP duplication leading to the origin of CP43 and CP47 subunits of photosystem IIdAB duplication leading to the origin of Alpha and Beta subunits of ATP synthaseΔT the span of time between dD0, dCP, dAB, or the LUCA, and the MRCA of Cyanobacteria MaMega-annum, million years GaGiga-annum, billion yearsν Rate of amino acid substitutions per siteδ Ga−1 Amino acid substitutions per site per billion years
Keywords
Origin of photosynthesis Origin of life Cyanobacteria Photosystem Reaction centre Water oxidation
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