Early Archean origin of heterodimeric Photosystem I

Tanai Cardona

doi:10.1016/j.heliyon.2018.e00548

Abstract

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.

Highlights

When and how oxygenic photosynthesis originated remains a highly debated subject with dates ranging from 3.8 billion years (Ga) [1, 2] to shortly before 2.4 Ga [3, 4], the onset of the Great Oxidation Event (GOE)
There could have been a gap of 600 million years (Ma) to more than 1.0 Ga between the origin of anoxygenic photosynthesis and the emergence of oxygenic photosynthesis
I have noted that the evolution of all reaction centre proteins, including those used in oxygenic photosynthesis, diversified early, rapidly, and in parallel [14]

Summary

Introduction

When and how oxygenic photosynthesis originated remains a highly debated subject with dates ranging from 3.8 billion years (Ga) [1, 2] to shortly before 2.4 Ga [3, 4], the onset of the Great Oxidation Event (GOE). Consistent with this, Cardona et al [13] demonstrated that the divergence of the anoxygenic Type II reaction centres from water-oxidising Photosystem II (PSII) occurred soon after the emergence of photosynthesis as the result of one reaction centre gaining or losing the structural domains required to oxidise water to oxygen, still at a homodimeric stage. Cardona et al [13] showed that one of the most ancient diversification events in the evolution of photosynthesis, after the divergence of Type I and Type II reaction centres, was the specific gene duplication of the ancestral watersplitting homodimeric core that permitted the heterodimerisation of PSII during the early Archean. It can be postulated that the gene duplication event that led to the heterodimerisation of PSI occurred after the evolution of water oxidation and was driven by the presence of oxygen.

Results and discussion

Bayesian relaxed molecular clock analysis

Horizontal gene transfer

Heterodimeric Photosystem I and oxygen

Final remarks

Materials and methods