Early Archean origin of Photosystem II

Abstract

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.

The Archean atmosphere

“…Phylogenetic analyses mostly suggest that cyanobacteria originated by 2.8 Ga. Molecular clocks must be calibrated by physical evidence, and phylogenetic methods are themselves debated. While some argue that oxygenic photosynthesis evolved only 50 to 100 Ma before the GOE (115), most studies suggest an earlier Paleoarchean or Mesoarchean age [e.g., (3,118,119)].…”

Active Galactic Nuclei: Boon or Bane for Biota?

“…The origin of oxygenic photosynthesis remains less tightly constrained, with some proxies (e.g., U-Th-Pb isotopic ratios) placing it as far back as 3.7 Ga (Rosing & Frei 2004), although unambiguous evidence from microfossils appears to date back only to 1.9 Ga (Lyons et al 2014;Fischer et al 2016). Despite this uncertainty, there are multiple grounds for contending that oxygenic photosynthesis may have evolved by 2.7 Ga, based on isotopic ratios, phylogenetics and microfossils (Buick 2008;Schirrmeister et al 2016), thus amounting to its emergence by at least several 100 Myr prior to the Great Oxidation Event at ∼ 2.4 Ga; see also Knoll et al (2016); Lingam & Loeb (2019c); Cardona et al (2019). In toto, it is not altogether unreasonable to surmise that both anoxygenic and oxygenic photosynthesis might have evolved over a time span ranging from 10 8 to 10 9 yrs after the origin of life on Earth.…”

Evolutionary Implications of Anoxygenic Phototrophy in the Bacterial PhylumCandidatusPalusbacterota (WPS-2)

“…That the three different anoxygenic Type II reaction centers show distinct mechanisms of redox tuning on key positions around Bch M and other photochemical pigments could indicate that these lineages radiated soon after the L and M duplication. Furthermore, given that anoxygenic Type II reaction centers show up to five times faster rates of evolution than cyanobacterial PSII 30 and that the emergence of at least some of major clades of phototrophs with anoxygenic Type II reaction centers postdate the GEO 50 , it is possible that the duplication of L and M subunits, and the radiation of the known anoxygenic Type II reaction centers occurred after the origin of oxygenic photosynthesis 30 . Therefore, the idea that extant forms of anoxygenic phototrophy powered by heterodimeric Type II reaction centers represent a "primitive" form of photosynthesis is not supported by the available data.…”

“…A total of 14 L and 12 M amino acid sequences were collected from the compiled metagenome data. The sequences were added to a dataset of Type II reaction center subunits compiled before 30 , which included sequences from Cyanobacteria, Proteobacteria, and Chloroflexi. Sequence alignments were done in Clustal Omega 31 using 10 combined guide trees and Hidden Markov Model iterations.…”