The Great Oxygenation Event, the Origin of Oxygen Photosynthesis and Eukaryoote Emergence
Chris King

The great oxygenation event is one of the most significant geological transformations in Earth's history, in which the atmosphere began to have non-negligible amounts of molecular oxygen. On the bass of geological evidence, the GOE dates to around 2.4 billion years ago (Holland 2006). This dating corresponds to a time where it is assumed the oxygenic photosynthetic organisms had become numerous enough to globally affect the composition of the atmosphere, but it tells us little about the date at which oxygen photosynthesis, which requires a two photon process to split water actually evolved. Traditional assumptions are that cyclic photosynthesis involving only ATP generation as in some archaea and then lower energy photosystems, such as based on H2S, involving only a single type A or B photosystem preceded the photosynthetic apparatus found today in cyanobacteria.

Fig 1: O2 build-up in the Earth's atmosphere. Red and green lines represent the range of the estimates while time is measured in billions of years ago (Ga). Stage 1 (3.85–2.45 Ga): Practically no O2 in the atmosphere. The oceans were also largely anoxic with the possible exception of O2 gases in the shallow oceans. Stage 2 (2.45–1.85 Ga): O2 produced, and rose to values of 0.02 and 0.04 atm, but absorbed in oceans and seabed rock. Stage 3 (1.85–0.85 Ga): O2 starts to gas out of the oceans, but is absorbed by land surfaces. There was no significant change in terms of oxygen level. Stages 4 and 5 (0.85–present): O2 sinks filled and the gas accumulates.

Contrasting this date is an earlier date for the major expansion of genetic diversity, which shows an explosion of the key genes occupying central metabolic pathways beginning around 3.3 billion years ago, including electron transport components. Since photosynthesis is central to respiration as a heterotrophic electron transport metabolism, the logical conclusion is that the key genetic pathways for photosynthesis evolved around 3.3 billion years ago, and given the eventual global predominance of oxygen photosynthesis and the two photoreceptor system it requires this should also date more closely to the earlier date.

Fig 2: Tree diagram of the birth, transfer, duplication and loss of key genes in the redox and electron transport pathways, in a founding burst of gene evolution between 3.3 and 2.7 billion years ago (David and Alm 2010).

However shotgun analysis of multiple uncultured genomes from a variety of sources have established that cyanobacteria are part of a much larger group of organisms, and that the photosynthetic branch now called the Oxyphotobacteria appear to have evolved from a common ancestor that did not possess the photosyntheitc machinery of current cyanobacteria.

Fig 3: Phylogenetic trees of the phylum Cyanobacteria. (a) A maximum likelihood tree of the phylum Cyanobacteria based on the concatenated alignment of 83 phylogenetically conserved proteins. Putative acquisitions of photosystem and flagella genes are indicated by colored arrows. (b) A maximum likelihood tree based on 16S rRNA genes from the class Melainabacteria obtained by Di Rienzi et al. (2013) and this study, together with public representatives from the Greengenes database version 13_05 and Silva 115 database (Soo et al. 2015).

Fig 4: Evolution of photosynthesis and aerobic respiration in Cyanobacteria. The Cyanobacteria are inferred to be ancestrally nonphototrophic and acquired the ability for photosynthesis (PSI and PSII) after the divergence of the Oxyphotobacteria from the Melainabacteria. The three Cyanobacteria classes likely acquired aerobic respiration independently after the rise of oxygen (atmospheric oxygen is represented by the red shading). Squares and triangles indicate acquisitions of complex III, whereas circles and diamonds indicate acquisitions of complex IV. Oxyphotobacteria acquisitions are shown in green (top), Melainabacteria acquisitions in blue and purple (middle), and Sericytochromatia acquisitions in red and pink (bottom) (Soo et al. 2017).

Shih et al. (2017) making a further analysis of these newly discovered branches concurs that crown group Oxyphotobacteria evolved ca. 2.0 billion years ago, well after the rise of atmospheric oxygen. They estimate the divergence between Oxyphotobacteria and Melainabacteria to ca. 2.5-2.6 billion years ago, which – if oxygenic photosynthesis is an evolutionary a product of the Oxyphotobacteria – marks an upper limit for the origin of oxygenic photosynthesis, and on the basis of these results state they are consistent with oxygenic photosynthesis having evolved relatively close in time to the rise of atmospheric oxygen.

Fig 5: Left: Complete labeled 16S rDNA tree of the Cyanobacterial phylum. Class Oxyphotobacteria in green, class Melainabacteria (orders Gastranaerophilales, Obscuribacterales, Vampirovibrionales, Caenarcaniphilales) in blue, and ML635J-21 clades shown in red. The majority of these Melainabacteria and ML635J-21 sequences were collected from aphotic and anaerobic environments, consistent with the physiologies reconstructed from existing Melainabacteria genomes. Right: Divergence time estimates for the Cyanobacterial phylum. Dated phylogeny generated from cross-calibrated Bayesian analysis of a concatenated dataset (Run T65). The alignment is composed of conserved proteins found in plastids, mitochondria, and bacteria as well as their 16S rDNA sequences. All analyses illustrate that crown group Oxyphotobacteria postdate the rise of oxygen, which in turn reflects O2 sourced from stem group lineages ( Shih et al. 2017).

However Cardona (2018) has investigated the evolutionary tree of Photosystem I one of the two photosystems necessesary for oxygenic photosynthesis. A unique trait of oxygenic photosynthesis is that the process uses a Type I reaction centre with a heterodimeric core, 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. The paper shows 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.

Fig 6 Left: Maximum Likelihood tree of Type I reaction centre proteins. The tree is characterised by a deep split of reaction centre proteins, which separates those employed in anoxygenic phototrophy from those employed in oxygenic photosynthesis (grey spot). All extant Cyanobacteria descended from a common ancestor that already had highly divergent PsaA and PsaB subunits (red spot). The gene duplication that led to PsaA and PsaB occurred at an earlier point in time (orange spot), which predated the most recent common ancestor of Cyanobacteria by an unknown period of time. It is hypothesised that the gene duplication that led to PsaA and PsaB occurred as a specialisation to oxygenic photosynthesis, therefore water oxidation should have originated before this gene duplication event (arrow). Right: Bayesian relaxed molecular clock of Type I reaction centres. The tree was calculated assuming that Type I reaction centres had originated by 3.5 Ga (grey dot). The orange dot indicates the duplication event that allowed the divergence of PsaA and PsaB. Red dots highlight the nodes that were calibrated as described in Materials and Methods. The light grey bars along the nodes show the uncertainty, 95% con- fidence interval, on the estimated divergence time. Sequences marked as hA denote those from strains of Heliobacteria, while those marked as cA from Chlorobi and Acidobacteria. Sequences marked as A and B represent PsaA and PsaB from Cyanobacterial and eukaryotic PSI. The blue bar marks the GOE.

In a previous paper, Cardona (2017), showed that photosystem II is a chimera of reaction centers, with an origin early in the Archaean. Consistent with this, Cardona et al. (2017) have 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 and have also shown 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 water-splitting homodimeric core that permitted the heterodimerisation of PSII during the early Archean.

Fig 7: Relaxed molecular clock of Type II reaction center proteins. Red dots are calibration points. The gray dot denoted II, represents the ancestral Type II reaction center protein. The orange dot (D0) marks the initial divergence of D1 and D2. The violet dot marks the divergence point between G2 atypical D1 sequences and standard D1. The green dot marks the divergence point between the microaerobic D1 forms (G3) and the dominant form of D1 (G4). The blue dot represents the origin of the dominant form of D1 inherited by all extant Cyanobacteria and photosynthetic eukaryotes. The gray bars represent the standard error of the estimated divergence times at the nodes. The orange bar shows the GOE

Cyanobacteria enter the fossil record in the form of stromatolite mats around 3.5 billion years ago. William Schopf (Scientific American Feb 1991) found remnants of 3.6 billion-year-old stromatolites lying near fossils of 3.5 billion-year-old cells that resemble modern cyanobacteria, forming strings of putative microscopic cells. In 2016 (Nutman et al. 2016) discovered putative stromatolites dating to 3.7 billion years in the Isua formation, in Greenland. Thus oxygen-generating photosynthesis which provides an energetic basis for eucaryote respiratory metabolisms to survive arose very early.

Before the Great Oxidation Event (GOE) 2.4–2.2 billion years ago it has been traditionally thought that oceanic water columns were uniformly anoxic due to a lack of oxygen-producing microorganisms. Recently, however, it has been proposed that transient oxygenation of shallow seawater occurred between 2.8 and 3.0 billion years ago. Satkoski et al. (2015) present Fe and U–Th– Pb isotope data that demonstrate significant oxygen contents in the shallow oceans at 3.2 Ga, based on analysis of the Manzimnyama Banded Iron Formation (BIF), Fig Tree Group, South Africa again consistent with an earlier emergence of oxygenic photosynthesis.

An investigation (Blättler et al. 2018) from a remarkably preserved ~2.0 billion years old marine marine salt bed evaporite sucession bearing carbonates, sulfates, halites, and bittern salts, from the Onega Basin in Russian Karelia, shows that the evaporite minerals provide a robust constraint that marine sulfate concentrations were at least 10 mmol/kg, representing an oxidant reservoir equivalent to over 20% of the modern ocean-atmosphere oxidizing capacity. These results show that substantial amounts of surface oxidant accumulated during this critical transition in Earth's oxygenation. Today, marine sulfate constitutes one of the largest surface oxidant reservoirs, equivalent to almost twice the modern atmospheric O2 inventory. This shows that the great oxidation event was not a trickle, but a major floo,d altering the composition of the planet's chemistry and chemical cycles.

An intriguing idea is that the rise in oxygen levels, in the great oxygenation event, due to cyanobacterial photosynthesis in ancient Archean microenvironments, drove the transformation of an archaeal lineage into the first eukaryotes through a combination of much greater respiratory yields arising from mitochondrial endosymbiosis and increased stresses due to reactive oxygen species. Selective pressure for efficient repair of ROS/UV-damaged DNA drove the evolution of sex, which required cell-cell fusions, cytoskeleton-mediated chromosome movement, and emergence of the nuclear envelope. The model implies that evolution of sex and eukaryogenesis were inseparable processes (Gross & Bhattacharya 2010).

Kipp et al. (2017) investigating fluctuations in oxygen levels around the GOE due to oxidative weathering in coastal regions note that recognition of oxygen-rich conditions in the early Paleoproterozoic opens up the possibility that there was a relatively long (∼200 My) interval that may have been favorable for the evolution of complex life forms long before the fossil record indicates their rise to ecological importance. Although convincing fossil evidence of multicellular eukaryotic life is hard to come by in the Proterozoic, the researchers note that there are numerous reports of fossils purported to have eukaryotic affinity that span nearly the entire temporal extent of the Proterozoic. These include centimeter-scale structures in the ∼2.1 Ga Francevillian Series of Gabon that have been interpreted as populations of multicellular organisms.


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