Anoxygenic Type‐I Photosystems and Evolution of Photosynthetic Reaction Centers

Hohmann‐Marriott, Martin F.; Blankenship, Robert E.

doi:10.1002/9783527623464.ch13

Cited by 12 publications

(8 citation statements)

References 110 publications

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“…Mirroring the evolution of Type II reaction centers, a molecular clock study on Type I reaction centers showed that the duplication event that led to the heterodimerization of the core of Photosystem I was also more likely to be the oldest node after the root (Cardona et al, 2012). This duplication event is widely accepted to have been an evolutionary adaptation to oxygenic photosynthesis (Ben-Shem, Frolow, & Nelson, 2004;Hohmann-Marriott & Blankenship, 2008;Rutherford et al, 2012) and was found to predate the earliest diversification event of anoxygenic Type I reaction centers (Cardona, 2018); namely, the divergence of the reaction center of Heliobacteria from that which gave rise to those in phototrophic Chlorobi and Acidobacteria.…”

Section: An Extended C-terminus and The Mn 4 Cao 5 Cluster Binding mentioning

confidence: 99%

Early Archean origin of Photosystem II

et al. 2018

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Photosystem II is a photochemical reaction center that catalyzes the light‐driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here, we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale, we hypothesize that this early Archean photosystem was capable of water oxidation to oxygen and had already evolved protection mechanisms against the formation of reactive oxygen species. This would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.

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Section: An Extended C-terminus and The Mn 4 Cao 5 Cluster Binding mentioning

confidence: 99%

Early Archean origin of Photosystem II

et al. 2018

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“…1 ). It is thought that the heterodimerisation process was an evolutionary response to oxygen [ 16 , 17 , 18 ]. For example, it was proposed that the asymmetric fine-tuning of the redox cofactors allows back electron transfer reactions to occur safely, minimising the formation of triplet chlorophyll states that can lead to the production of reactive oxygen species [17] .…”

Section: Introductionmentioning

confidence: 99%

Early Archean origin of heterodimeric Photosystem I

Cardona

2018

Heliyon

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When and how oxygenic photosynthesis originated remains controversial. Wide uncertainties exist for the earliest detection of biogenic oxygen in the geochemical record or the origin of water oxidation in ancestral lineages of the phylum Cyanobacteria. A unique trait of oxygenic photosynthesis is that the process uses a Type I reaction centre with a heterodimeric core, also known as Photosystem I, made of two distinct but homologous subunits, PsaA and PsaB. In contrast, all other known Type I reaction centres in anoxygenic phototrophs have a homodimeric core. A compelling hypothesis for the evolution of a heterodimeric Type I reaction centre is that the gene duplication that allowed the divergence of PsaA and PsaB was an adaptation to incorporate photoprotective mechanisms against the formation of reactive oxygen species, therefore occurring after the origin of water oxidation to oxygen. Here I show, using sequence comparisons and Bayesian relaxed molecular clocks that this gene duplication event may have occurred in the early Archean more than 3.4 billion years ago, long before the most recent common ancestor of crown group Cyanobacteria and the Great Oxidation Event. If the origin of water oxidation predated this gene duplication event, then that would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.

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“…This is a trait that has been retained by all oxygenic phototrophs. A heterodimeric Photosystem I is a distinctive and exclusive characteristic of oxygenic photosynthesis and it is widely accepted that the heterodimerisation of the core was an adaptation to oxygenic photosynthesis [29,67,68]. PsaA and PsaB, the core subunits of Photosystem I share about 43% sequence identity: this is true across the entire diversity of oxygenic phototrophs from the earliest branching Cyanobacteria to the most exotic variety of avocado, which implies that the mrca of Cyanobacteria inherited a heterodimeric Photosystem I that had PsaA and PsaB with about 43% identity.…”

Section: Easy Transfermentioning

confidence: 99%

Thinking Twice about the Evolution of Photosynthesis

Cardona¹

2019

Preprint

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Sam Granick opened his seminal 1957 paper titled Speculations on the Origins and Evolution of Photosynthesis with the assertion that there is a constant urge in human beings to seek beginnings (I concur). This urge has led to an incessant stream of speculative ideas and debates on the evolution of photosynthesis that started in the first half of the twentieth century and shows no signs of abating. Some of these speculative ideas have become common place, are taken as fact, but find little support. Here I review and scrutinise three widely accepted ideas that underpin the current study of the evolution of photosynthesis: firstly, that the photochemical reaction centres used in anoxygenic photosynthesis are more primitive than those in oxygenic photosynthesis; secondly, that the probability of acquiring photosynthesis via horizontal gene transfer is greater than the loss of photosynthesis; and thirdly, and most importantly, that the origin of anoxygenic photosynthesis predates the origin of oxygenic photosynthesis. I shall attempt to demonstrate that these three ideas are often grounded on incorrect assumptions built on more assumptions with no experimental nor observational support. I hope that this brief review will not only serve as cautionary tale, but also that it will open new avenues of research aimed at disentangling the complex evolution of photosynthesis and its impact on the early history of life and the planet.

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Anoxygenic Type‐I Photosystems and Evolution of Photosynthetic Reaction Centers

Cited by 12 publications

References 110 publications

Early Archean origin of Photosystem II

Early Archean origin of Photosystem II

Early Archean origin of heterodimeric Photosystem I

Thinking Twice about the Evolution of Photosynthesis

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