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Origin and evolution of water oxidation before the last common ancestor of the Cyanobacteria

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Title: Origin and evolution of water oxidation before the last common ancestor of the Cyanobacteria
Authors: Cardona Londono, T
Murray, JW
Rutherford, AW
Item Type: Journal Article
Abstract: 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 (Mn4CaO5) 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 Mn4CaO5 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 Mn4CaO5 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 towards the innovation and optimization of water oxidation before the last common ancestor of all known cyanobacteria.
Issue Date: May-2015
Date of Acceptance: 1-Feb-2015
URI: http://hdl.handle.net/10044/1/19201
DOI: 10.1093/molbev/msv024
ISSN: 1537-1719
Publisher: Oxford University Press (OUP)
Start Page: 1310
End Page: 1328
Journal / Book Title: Molecular Biology and Evolution
Volume: 32
Issue: 5
Copyright Statement: © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 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
Sponsor/Funder: Biotechnology and Biological Sciences Research Council (BBSRC)
Biotechnology and Biological Sciences Research Council (BBSRC)
Funder's Grant Number: BB/K002627/1
BB/F023308/1
Keywords: Science & Technology
Life Sciences & Biomedicine
Biochemistry & Molecular Biology
Evolutionary Biology
Genetics & Heredity
water oxidation
Photosystem II
PsbA
cyanobacteria
oxygenic photosynthesis
GLOEOBACTER-VIOLACEUS PCC-7421
AMINO-ACID-RESIDUES
PHOTOSYNTHETIC REACTION CENTERS
FTIR DIFFERENCE SPECTROSCOPY
ELECTRON-ACCEPTOR COMPLEX
EVOLVING PHOTOSYSTEM-II
GENE-EXPRESSION
D1 PROTEIN
PSBA GENE
THERMOSYNECHOCOCCUS ELONGATUS
Photosystem II
PsbA
cyanobacteria
oxygenic photosynthesis
water oxidation
Cyanobacteria
Evolution, Molecular
Light
Oxidation-Reduction
Oxygen
Photosynthesis
Photosystem II Protein Complex
Water
Cyanobacteria
Oxygen
Water
Photosystem II Protein Complex
Evolution, Molecular
Photosynthesis
Oxidation-Reduction
Light
Evolutionary Biology
0601 Biochemistry and Cell Biology
0603 Evolutionary Biology
0604 Genetics
Publication Status: Published
Online Publication Date: 2015-02-04
Appears in Collections:Faculty of Natural Sciences



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