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http://bioscience.oxfordjournals.org March 2016 / Vol. 66 No. 3 • BioScience 189

BioScience 66: 189–195. © 2016 Blaustein. All rights reserved. doi:10.1093/biosci/biv193

The Great Oxidation Event

RICHARD BLAUSTEIN

Evolving understandings of how oxygenic life on Earth began

Earth history has many tipping points, some that are regional and

others that are global and epoch defin-ing. None was as all encompassing as the Great Oxidation Event (GOE), a geological episode occurring around 2.35 billion years ago. With the GOE, the atmosphere switched from being oxygen free to having a small percent-age of oxygen that would hold for 1.5 billion years, at which point a sec-ond leap in oxygen occurred, around 700 million years ago. The GOE’s net effect is widespread oxygenic photo-synthesis and, subsequently, oxygen-breathing organisms from which descended diverse multicelled and complex life. Sophisticated new isoto-pic analyses, as well as cross-disciplin-ary work by geochemists, biochemists, geologists, and others, are fueling a fresh examination of the GOE. By better understanding the early oxygen-ation of the planet, researchers say, sci-entists can find answers to the origins of complex life.

In 2013, the National Science Foundation (NSF) launched the Early Oxygen initiative (www.earlyo2.org), a 5-year effort by 21 US researchers to unravel “one of the major mysteries” in Earth science, focusing particularly on the role the Earth’s interior played in the GOE. “The GOE is probably the most fundamental transformation in the history of the planet, aside from the origin of life itself,” says Arizona State geochemist Ariel Anbar, who leads the initiative. “But we still don’t really understand fully how it happened.”

The GOE has wide-ranging impli-cations. “Once you have enough O2 in the atmosphere, you change the dominant metabolic strategies; meta-bolic networks rearrange,” putting life on an oxygen-breathing path to complexity, Anbar adds. Eukaryotic organisms, species with complex cell arrangements allowing for multicellu-lar life, appear for the first time in the fossil record at 1.8 billion years ago, not long (geologically speaking) after a noted period during which oxygen concentration spiked: the Lomagundi

excursion 2.3 billion to 2.1 billion years ago.

Early Oxygen researchers and many other scientists are investigating how oxygenation occurred within the biosphere, using refined isotopic tools on geological samples and examining biological features, such as on stromat-olites, the ancient mineralized remains of mats of bacteria. This GOE inves-tigation has three prongs. The first looks at the biochemistry of oxygenic photosynthesis and how it evolved to be the energy driver of cyanobacteria,

Stromalotites result from the mineralization of layers upon layers of bacteria and are morphological examples of structures that come about via physical,

chemical, and biological actions. This stromatolite, found in South African, is an estimated 2.98 billion years old. Photograph: Tonja Bosak.

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190 BioScience • March 2016 / Vol. 66 No. 3 http://bioscience.oxfordjournals.org

the organisms that produced the Earth’s early oxygen. This inquiry also explores how oxygenic photosynthesis branched off from anoxygenic photo-synthesis. Questions remain, but the biochemical study of how oxygenic photosynthesis evolved is a starting point for understanding the history of the Earth–oxygen relationship.

A second and very hearty line of research tries to spot when oxygenic photosynthesis first occurred and turns to ancient rocks, soils, and stromatolites for evidence. Scientists now generally agree that cyanobacteria were active hundreds of millions of years before the GOE, generating either nonag-gregating oxygen “whiffs”—transient oxygen released into the atmosphere—or “oases,” which are small oxygenated pockets in the shallow ocean surface or under rocks in the very little landmass that was present. The dominant pre-GOE gases in the air, especially meth-ane, would quickly neutralize these oxygen releases. In fact, in August 2015, a team led by researchers from the University of Wisconsin–Madison made news by publishing a paper in Earth and Planetary Science Letters that offered evidence of oxygenic pho-tosynthesis from 3.2 billion years ago in ancient South Africa rocks. Their finding is in the middle of recent esti-mates, from Danish geologist Minik Rosing’s controversial 2003 claim of 3.8-billion-year-old oxygen photosyn-thesis signs in Greenland’s Isua rocks to a recent dating of 3.0 billion years ago that used advanced molybdenum techniques.

University of California, Riverside, geochemist Timothy Lyons, also on the NSF project, coauthored a 2014 Nature paper that surveyed oxygen history on Earth, from the early releases up to the GOE and its after-math. Lyons emphasizes that the pre-GOE signs of cyanobacteria activity are important because they indicate that Earth’s oxygen narrative is a more protracted affair.

The third line of investigation looks at the diverse geological and biological factors that converged to produce the GOE tipping point. This

interdisciplinary line of research looks at plate tectonics, crust and continent formation, volcanic activity, the inte-rior Earth’s geochemistry, weathering changes on the Earth surface, and cyanobacteria activity—all coming together as the enabling backdrop for the big GOE change that established

a permanent oxygen presence in the atmosphere.

Biology and geology interacted and transformed each other, according to Lyons. “The reality is that the envi-ronment dictates the course of life, when at the same level, life dictates the course of the environment,” Lyons

Washington University biochemist Bob Blankenship has a longstanding interest in the origins of oxygenic photosynthesis. Here, he holds up a sample

of cyanobacteria, the bacteria that started oxygenic photosynthesis at least 2.35 billion years ago. Photograph: Joe Angeles/WUSTL Photo.

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says. “So there is this big coevolution, and what could be a bigger representa-tion of this than the oxygenation of the biosphere? That is a big life step.”

Cyanobacteria: The great innovatorsBiochemist Robert Blankenship of Washington University in St. Louis has researched photosynthesis since the 1970s and points out that anoxygenic photosynthesis definitely preceded the oxygenic variety. All photosynthesis originates with bacteria, Blankenship notes, and of the seven major groups of photosynthetic bacteria, six are anoxygenic, whereas only one is oxy-gen evolving—the cyanobacteria. Blankenship says that the oxygen pho-tosynthesis found today in trees and algae, for example, has not changed fundamentally from when it began with cyanobacteria. “Obviously, there have been some refinements of one type or another, but the basic mecha-nism was almost certainly there 2.4 billion [years ago] or an even earlier time frame”—that is, before the GOE.

Oxygenic photosynthesis is more complex and productive than anoxy-genic photosynthesis. Unlike anoxy-genic photosynthesis with a single photosystem—the biochemical path-way for capturing light and creating energy—oxygenic photosynthesis links two, known as photosystems 1 and 2. In photosystem 2, the first part of the two-part biochemical system (but called photosystem 2 because it was identified after photosystem 1), a unique oxygen-evolving complex has a cluster of four manganese mole-cules, which break oxygen from water and set water as an electron donor in the biochemical chain. According to Blankenship, the development of the oxygen-evolving complex was a genuine hurdle for evolution. “For a lot of biochemical systems, you’ll find that nature has figured how to skin the cat several different independent times,” Blankenship explains. “Here, it seems not to be the case. It seems the ability to oxidize water to molecular oxygen only appeared once during the course of evolution.” He adds, “That is

testament to the fact that chemically, it is a very difficult problem and thing to do,” especially because the water bond is hard to break.

The advantages of oxidizing water are twofold. First, anoxygenic photo-synthesis may rely on iron, hydrogen, or other electron sources, and those substances could have become sparse in some locations, such as hydrother-mal vents. But on the Earth, water is nearly unlimited. Furthermore, as

Blankenship explains, oxygenic pho-tosynthesis attains the maximum bio-chemical energy, unlike anoxygenic photosynthesis. “So once you made that transition to oxygenic photosyn-thesis,” Blankenship says, “you get the biggest bang for your buck in terms of being able to use that energy at later points.”

Blankenship says one big open question is how the two photo-systems emerged from an anaerobic

University of California, Riverside, geochemist Timothy Lyons here visits the Australian Pilbara site that is noted for its ancient soils and rocks dating back

to the Archean eon, from 2.5 billion to 4.0 billion years ago. Pilbara has offered geological samples that contain evidence of oxygenic photosynthesis before the

Great Oxidation Event. Photograph: Ariel Anbar.

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photosynthetic organism, diverged, and then converged again in cyano-bacteria, perhaps through some kind of horizontal gene transfer, much like the endosymbiosis that transformed cyanobacteria into chloroplasts in plants. Another challenging question, says Blankenship, is this: Given that oxygen is toxic for anaerobic organ-isms, how did life survive it? “You really have to have a coevolution of the ability to make oxygen and do oxy-genic photosynthesis and the ability to protect yourself against the oxygen that you make and the deleterious effects that you have from that.” Blankenship suggests that perhaps there was a rudi-mentary oxygen defense already in place or else that the development of the defense ran parallel with oxygenic photosynthesis in cyanobacteria.

University of Alberta geobiologist Kurt Konhauser says the biochemi-cal work of Blankenship and others is important for understanding the GOE. Whereas these researchers look at the mechanisms that would have led from one type of photosynthesis to another, others are looking at how photosyn-thesizers survive different kinds of modern environments, Konhauser says. By combining the modern with the biochemical, scientists now can better interpret the past. “From that, we can use that information to under-stand the rock record,” he says.

Whiffs, oases, stromatolites—oxygen before 2.5 billion years agoWhen oxygenic photosynthesis began is key to understanding the oxygen narrative and how transient oxygen releases transformed into a permanent presence in the atmo-sphere and ocean. In recent years, researchers have cited evidence for the 2.5-, 2.7-, 3.0-, and, most recently, 3.2-billion-year-old traces of oxy-genic photosynthesis. These have been primarily based on isotope analysis. However, in one prominent case in which 2.7-billion-year-old rocks were determined to have what are called “biosignature” signs—molecules that were thought to be produced only

by organic activity—a follow-up study team, which included the “biosigna-ture” scientists, concluded that the specimens were contaminated from a later era. Additionally, Blankenship’s line of research points out that some ancient biological traces associated with oxygenic photosynthetic organ-isms could have been produced by early anoxygenic species. That left

most of the focus on geochemical and isotope techniques as the way to find oxygen production in ancient rocks.

For example, a study led by Anbar looked at 2.5-billion-year-old rock samples from the Pilbara region of Australia. Anbar’s team focused on molybdenum isotopes to substan-tiate that the rocks showed signs of ancient oxygenic photosynthesis.

Massachusetts Institute of Technology geobiologist Tanja Bosak and colleague Malcolm Walter studying the oldest site of stromatolites in Australia.

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Molybdenum has a certain isoto-pic pattern that can arise only in the presence of oxygen, and this was detected in the rocks. A late 2015 paper looked at osmium iso-topes for the same geological sample, confirming the earlier molybdenum findings.

Similarly, for a recent 3.0-billion-year claim of oxygenic photosynthesis, at the Pongola site in South Africa, Lyons’s group relied on molybdenum isotopes for telltale signs of oxygenic photosynthesis. A different team col-laborated on the 3.0-billion-year claim for that site using chromium isotopes. “What is most important to me is that we are pushing that back pretty far,” Lyons says. “For hundreds of millions of years pre-GOE, there are increasing diverse kinds of date information that indicate early production and at least transient accumulation of O2 in the atmosphere.”

Stromatolites are also an impor-tant focus of early oxygenic photo-synthesis. Massachusetts Institute of Technology geobiologist Tanja Bosak, also part of the NSF group, looks at the shapes and arrangements of the stro-matolites—the morphology—rather than isotopic signatures for assessing photosynthesis type. At the beginning of this decade, she and her colleagues looked at a 2.9-billion-year-old stro-matolite formation in the Pongola region and observed how the assem-blage of shapes and textures appar-ently matched cyanobacteria patterns. If accurate, this would be an early date for detecting oxygenic photosynthesis and stromatolites. Stromatolites are found around the world, and other sites may shed light on the GOE inves-tigation. Bosak also looked at modern stromatolite analogs to this sample, and she studied the spacing aspects of the South African stromatolite, which, according to Bosak, pointed to nutri-ent diffusion, competition, and diur-nal patterns that indicate oxygenation. For Bosak, the mineralized features that implied gas bubbles tipped the scale in favor of oxygenic photosyn-thesis. With the other evidence of structure and spacing and the type

of mineralization of this stromatolite, Bosak says, “Really, oxygenic photo-synthesis came up as the only likely candidate.”

As with other findings, this stromat-olite case is not conclusive. As new iso-topic techniques emerge, stromatolites

could be a focus of the convergence of isotopic and morphological tech-niques for GOE research, according to Konhauser. Bosak also hopes that more unconventional lines of investi-gation, such as simulations that recre-ate ancient environments, will become

Vivid red rocks and soils, such as those in these photos of the Australian Pilbara region, are emblematic of the Great Oxidation Event (GOE). The red

color indicates iron being oxidized. Heinrich Holland, who studied and coined the Great Oxidation Event, pointed to this type of red rocks and soils as a

cornerstone example of the GOE. Photographs: Ariel Anbar.

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an increasing part of the early-life exploration.

Enter the GOEWhereas most researchers now think that cyanobacteria produced oxygen before the GOE, the GOE remains firmly established as a definite cross-ing point in Earth history: It is where the oxygen presence was not erased but reached a level in the atmosphere that would grow and eventually undergird the evolutionary expan-sions of the past 700 million years. Konhauser, who says that the GOE date should be pushed back around 100 million years to 2.45 billion years ago, highlights the importance for the GOE by pointing out the concurrent increase of red-banded iron forma-tions, which are ancient rocks that indicate oxygen (or some other chem-ical that acts like oxygen) attaching to Earth’s abundant iron (as happens with rust). Red-banded iron forma-tions significantly increased around the time of the GOE, indicating a profound change in Earth chemistry. “Before that, we already have oxygen production,” Konhauser explains. “But the O2 that was produced was simply not sufficient to oxidize all the things in the environment around it, whether it be reduced iron in the oceans, . . . hydrogen gas coming out of volca-noes, . . . [or] methane produced by. . . bacteria.” He adds, “There’s a litany of different things. What the GOE seems to represent is that tip-ping point. Suddenly, we are now at a point where oxygen accumulates in the atmosphere, because there is more of it than the stuff that was stripping it out.”

In the early GOE thinking, the abundance of red-banded iron forma-tions was prime evidence for oxygen accumulation and the GOE. These formations are still a very important part of the GOE picture, but they are not conclusive evidence of oxygen-ation, because they appear later in the geological record. Moreover, the red transformation can also be produced from other geochemical (oxidizing) processes without oxygen.

In the early 2000s, University of Maryland geologist James Farquhar, working with Mark Thiemens, published findings on sulfur isotopes, which definitively show an irreversible aggregation of oxygen in the atmo-sphere. Farquhar’s research illustrated that sulfur isotopes in the Earth’s early atmosphere fractionate in a depend-able way, but when oxygen is in the atmosphere and there is consequently an ozone layer, the fractionation disap-pears because the ozone blocks ultra-violet rays. Lyons says that Farquhar and Thiemens’s research showed that about 2.3 billion to 2.4 billion years

ago, sulfur fractioning just turned off. “The data is quite stark and vivid,” Lyons says. “It helps you hang the GOE on a time, and it is calibrated with real levels of O2 in the atmosphere.”

The sulfur-isotopes measurements establish what would be the minimum level of atmospheric oxygen at the time of the GOE; this bottom figure is 0.001 percent of our current oxygen level. That may seem low—and the actual level is probably higher—but it is a base figure. Moreover, huge oxygen rises appear to have occurred during the Lomagundi excursion of 2.3 billion to 2.1 billion years ago,

Australia’s Pilbara region has supplied some of the rocks and soil samples that indicate cyanobacteria activity and oxygen production preceding the Great

Oxidation Event by hundreds of millions of years. Photograph: Ariel Anbar.

Further reading.

Bell EA, Boehnke P, Harrison TM, Mao WL. 2015. Potentially biogenic carbon pre-served in a 4.1 billion-year-old zircon. Proceedings of the National Academy of Sciences 112: 14518–14521. doi:10.1073/pnas.1517557112.

Holland HD. 2006. The oxygenation of the atmosphere and oceans. Philosophical Transactions of the Royal Society B 361: 903–915.

Lyons TW, Reinhard CT, Planavsky N. 2014. The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506: 307–315.

Satkoski AM, Beukes NJ, Li W, Beard BL, Johnson CM. 2015. A redox-stratified ocean 3.2 billion years ago. Earth and Planetary Science Letters 430: 43–53. doi:10.1016/j.epsl.2015.08.007.

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with global carbon isotopic measure-ments indicating an oxygen rise to perhaps 50 percent of current lev-els. Afterwards, according to Lyons’s research, a deep drop in oxygen appar-ently occurred, but not to the pre-GOE level.

A lot of activity converged around the GOE to produce oxygen on Earth’s surface. Certainly, the proliferation of cyanobacteria was crucial. Influential work on the early atmosphere by Penn State Earth scientists James Kasting and Lee Kump helps frame a pic-ture of a less potent atmosphere mix-ture that may not have smothered the oxygen produced by small islands of cyanobacteria around the GOE time. And volcanoes may have shifted from submarine to surface locations, alter-ing gas composition. Anbar’s Early Oxygen team is extending this line of investigation, with one group looking at whether the geochemistry of Earth’s interior altered the surface chemistry or whether surface changes—such as the subduction of surface crust into the interior—might have altered the interior emissions, which would have affected oxygen accumulating on the surface. It could have been a two-way street, according to Anbar.

Other important factors within the GOE convergence are the escape into outer space of hydrogen, the light-est element (perhaps from volcanoes and water split by photosynthesis), which favors oxygen accumulation, a finding articulated by University of Washington geochemist David Catling, and the critical increase of carbon burial, especially in the oceans, which sequesters the carbon that would have tied down free oxygen.

The change of the extant volca-noes, their released gases, and carbon burial are all associated with plate tectonics and land formation, which is an integral part of the early-oxygen

investigation. “One of the most excit-ing things for me,” says Lyons, “is that we are finally bridging to the tectonics community. . . . Tectonics is important because it is about the nature of the gases coming out of the interior. But it also means fundamentally that we are creating land surface that did not exist before.” He adds that “plate tectonics give us new domains, new ecologies, affects nutrient recycling. . . all the things we are talking about” with the GOE.

University of Maryland geochemist Roberta Rudnick, another participant in the NSF collaboration, works on Earth crust and continent formation. Echoing Lyons, Rudnick says, “If. . . we are able to make a link between what was happening in the solid Earth with what was happening in terms of changing atmospheric composi-tion, I think that would be terrific.” Rudnick points out that there are a lot of uncertainties about conti-nents, above-sea-level crust, volca-noes, and plate tectonic activity over 2 billion years ago. However, she points to a well-known increase in 2.7 billion-year-old zircons—a staple focus for ancient-Earth studies—as one indication of a dynamic increase in Earth surface crust at this time. There is debate on this, but some think that around this time, plate tectonics began generating the land-masses. The plate tectonic activity also could have changed the locales of volcanoes, possibly pushing them above sea level, again changing their gas composition.

“I think it is an exciting time, actually, in the study of continents because. . . the community may be heading towards a consensus. . . that something fundamentally changed with the solid Earth around 3.0 billion to 2.7 billion years ago, just before the GOE,” Rudnick adds.

The implications are dramatic: dynamic plate tectonic activity at work, instigating a complex chain of Earth system changes, including expanding the continental shelf that supported cyanobacteria and helped bury carbon detritus, with more oxygen-friendly volcanic eruptions, new rock-weathering dynamics, and an abundance of reactions between oxygen and iron and other substances. Together, these set in motion the GOE tipping point.

The GOE legacyIt is hard to overstate the impact of the GOE on life on Earth. The research-ers commonly say that humanity is here because of it. Other wide-ranging effects are illuminating. For example, with oxygen accumulating globally, Blankenship suspects that there was likely a massive die-off of anaerobic microbes that lacked oxygen defenses and probably dominated pre-GOE life.

Konhauser, focusing on microbial life, thinks that with cyanobacteria and the GOE, the interlinking of envi-ronment and life is further under-scored. “There is no such thing as a water–rock interaction, per se. It is a water–rock–biofilm interaction,” Konhauser says. He emphasizes that with the temperature conditions that allow for the planet to maintain water, microbes drive biogeological reac-tions on and just below the Earth’s surface.

Not only do weathering and eco-logical niches formation take on new forms, according to Konhauser, but also the Earth is readied for the domi-nance of aerobic respiration and the eventual advent of complex life.

Richard Blaustein is a freelance science and environmental journalist based in Washington,

DC. On Twitter, he can be followed at @richblaustein.

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