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Origin and Evolution of Water Oxidation before the Last Common Ancestor of the Cyanobacteria

Photosystem II, the water oxidizing enzyme, altered the course of evolution by filling the atmosphere with oxygen. Here, we reconstruct the origin and evolution of water oxidation at an unprecedented level of detail by studying the phylogeny of all D1 subunits, the main protein coordinating the wate...

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Autores principales: Cardona, Tanai, Murray, James W., Rutherford, A. William
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4408414/
https://www.ncbi.nlm.nih.gov/pubmed/25657330
http://dx.doi.org/10.1093/molbev/msv024
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author Cardona, Tanai
Murray, James W.
Rutherford, A. William
author_facet Cardona, Tanai
Murray, James W.
Rutherford, A. William
author_sort Cardona, Tanai
collection PubMed
description Photosystem II, the water oxidizing enzyme, altered the course of evolution by filling the atmosphere with oxygen. Here, we reconstruct the origin and evolution of water oxidation at an unprecedented level of detail by studying the phylogeny of all D1 subunits, the main protein coordinating the water oxidizing cluster (Mn(4)CaO(5)) of Photosystem II. We show that D1 exists in several forms making well-defined clades, some of which could have evolved before the origin of water oxidation and presenting many atypical characteristics. The most ancient form is found in the genome of Gloeobacter kilaueensis JS-1 and this has a C-terminus with a higher sequence identity to D2 than to any other D1. Two other groups of early evolving D1 correspond to those expressed under prolonged far-red illumination and in darkness. These atypical D1 forms are characterized by a dramatically different Mn(4)CaO(5) binding site and a Photosystem II containing such a site may assemble an unconventional metal cluster. The first D1 forms with a full set of ligands to the Mn(4)CaO(5) cluster are grouped with D1 proteins expressed only under low oxygen concentrations and the latest evolving form is the dominant type of D1 found in all cyanobacteria and plastids. In addition, we show that the plastid ancestor had a D1 more similar to those in early branching Synechococcus. We suggest each one of these forms of D1 originated from transitional forms at different stages toward the innovation and optimization of water oxidation before the last common ancestor of all known cyanobacteria.
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spelling pubmed-44084142015-06-26 Origin and Evolution of Water Oxidation before the Last Common Ancestor of the Cyanobacteria Cardona, Tanai Murray, James W. Rutherford, A. William Mol Biol Evol Discoveries Photosystem II, the water oxidizing enzyme, altered the course of evolution by filling the atmosphere with oxygen. Here, we reconstruct the origin and evolution of water oxidation at an unprecedented level of detail by studying the phylogeny of all D1 subunits, the main protein coordinating the water oxidizing cluster (Mn(4)CaO(5)) of Photosystem II. We show that D1 exists in several forms making well-defined clades, some of which could have evolved before the origin of water oxidation and presenting many atypical characteristics. The most ancient form is found in the genome of Gloeobacter kilaueensis JS-1 and this has a C-terminus with a higher sequence identity to D2 than to any other D1. Two other groups of early evolving D1 correspond to those expressed under prolonged far-red illumination and in darkness. These atypical D1 forms are characterized by a dramatically different Mn(4)CaO(5) binding site and a Photosystem II containing such a site may assemble an unconventional metal cluster. The first D1 forms with a full set of ligands to the Mn(4)CaO(5) cluster are grouped with D1 proteins expressed only under low oxygen concentrations and the latest evolving form is the dominant type of D1 found in all cyanobacteria and plastids. In addition, we show that the plastid ancestor had a D1 more similar to those in early branching Synechococcus. We suggest each one of these forms of D1 originated from transitional forms at different stages toward the innovation and optimization of water oxidation before the last common ancestor of all known cyanobacteria. Oxford University Press 2015-05 2015-02-04 /pmc/articles/PMC4408414/ /pubmed/25657330 http://dx.doi.org/10.1093/molbev/msv024 Text en © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Cardona, Tanai
Murray, James W.
Rutherford, A. William
Origin and Evolution of Water Oxidation before the Last Common Ancestor of the Cyanobacteria
title Origin and Evolution of Water Oxidation before the Last Common Ancestor of the Cyanobacteria
title_full Origin and Evolution of Water Oxidation before the Last Common Ancestor of the Cyanobacteria
title_fullStr Origin and Evolution of Water Oxidation before the Last Common Ancestor of the Cyanobacteria
title_full_unstemmed Origin and Evolution of Water Oxidation before the Last Common Ancestor of the Cyanobacteria
title_short Origin and Evolution of Water Oxidation before the Last Common Ancestor of the Cyanobacteria
title_sort origin and evolution of water oxidation before the last common ancestor of the cyanobacteria
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4408414/
https://www.ncbi.nlm.nih.gov/pubmed/25657330
http://dx.doi.org/10.1093/molbev/msv024
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