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The Great Oxidation Event
RICHARD BLAUSTEIN
Evolving understandings of how oxygenic life on Earth began
E
arth history has many tipping
points, some that are regional and
others that are global and epoch defining. 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 percentage of oxygen that would hold for
1.5 billion years, at which point a second leap in oxygen occurred, around
700 million years ago. The GOE’s net
effect is widespread oxygenic photosynthesis and, subsequently, oxygenbreathing organisms from which
descended diverse multicelled and
complex life. Sophisticated new isotopic analyses, as well as cross-disciplinary work by geochemists, biochemists,
geologists, and others, are fueling a
fresh examination of the GOE. By
better understanding the early oxygenation of the planet, researchers say, scientists 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.”
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.
The GOE has wide-ranging implications. “Once you have enough O2
in the atmosphere, you change the
dominant metabolic strategies; metabolic networks rearrange,” putting
life on an oxygen-breathing path to
complexity, Anbar adds. Eukaryotic
organisms, species with complex cell
arrangements allowing for multicellular 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 stromatolites, the ancient mineralized remains
of mats of bacteria. This GOE investigation has three prongs. The first
looks at the biochemistry of oxygenic
photosynthesis and how it evolved to
be the energy driver of cyanobacteria,
BioScience 66: 189–195. © 2016 Blaustein. All rights reserved.
doi:10.1093/biosci/biv193
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the organisms that produced the
Earth’s early oxygen. This inquiry also
explores how oxygenic photosynthesis
branched off from anoxygenic photosynthesis. 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 nonaggregating 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 preGOE gases in the air, especially methane, 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 photosynthesis from 3.2 billion years ago
in ancient South Africa rocks. Their
finding is in the middle of recent estimates, from Danish geologist Minik
Rosing’s controversial 2003 claim of
3.8-billion-year-old oxygen photosynthesis 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 aftermath. Lyons emphasizes that the preGOE 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
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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.
interdisciplinary line of research looks
at plate tectonics, crust and continent
formation, volcanic activity, the interior 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 environment dictates the course of life,
when at the same level, life dictates
the course of the environment,” Lyons
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says. “So there is this big coevolution,
and what could be a bigger representation of this than the oxygenation of the
biosphere? That is a big life step.”
Cyanobacteria: The great
innovators
Biochemist 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 oxygen evolving—the cyanobacteria.
Blankenship says that the oxygen photosynthesis 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 mechanism 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 anoxygenic photosynthesis. Unlike anoxygenic photosynthesis with a single
photosystem—the biochemical pathway 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 molecules, 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
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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.
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 photosynthesis may rely on iron, hydrogen,
or other electron sources, and those
substances could have become sparse
in some locations, such as hydrothermal vents. But on the Earth, water
is nearly unlimited. Furthermore, as
Blankenship explains, oxygenic photosynthesis attains the maximum biochemical energy, unlike anoxygenic
photosynthesis. “So once you made
that transition to oxygenic photosynthesis,” 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
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photosynthetic organism, diverged,
and then converged again in cyanobacteria, 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 organisms, how did life survive it? “You
really have to have a coevolution of the
ability to make oxygen and do oxygenic 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 rudimentary 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 biochemical 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 photosynthesizers 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 understand the rock record,” he says.
Whiffs, oases, stromatolites—
oxygen before 2.5 billion
years ago
When oxygenic photosynthesis
began is key to understanding the
oxygen narrative and how transient
oxygen releases transformed into a
permanent presence in the atmosphere 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 oxygenic 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
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Massachusetts Institute of Technology geobiologist Tanja Bosak and colleague
Malcolm Walter studying the oldest site of stromatolites in Australia.
by organic activity—a follow-up study
team, which included the “biosignature” 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 organisms 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 substantiate that the rocks showed signs
of ancient oxygenic photosynthesis.
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Molybdenum has a certain isotopic pattern that can arise only in
the presence of oxygen, and this
was detected in the rocks. A late
2015 paper looked at osmium isotopes for the same geological sample,
confirming the earlier molybdenum
findings.
Similarly, for a recent 3.0-billionyear 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 collaborated 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 important focus of early oxygenic photosynthesis. Massachusetts Institute of
Technology geobiologist Tanja Bosak,
also part of the NSF group, looks at the
shapes and arrangements of the stromatolites—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 stromatolite formation in the Pongola
region and observed how the assemblage of shapes and textures apparently 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 investigation. 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 nutrient diffusion, competition, and diurnal patterns that indicate oxygenation.
For Bosak, the mineralized features
that implied gas bubbles tipped the
scale in favor of oxygenic photosynthesis. With the other evidence of
structure and spacing and the type
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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.
of mineralization of this stromatolite,
Bosak says, “Really, oxygenic photosynthesis came up as the only likely
candidate.”
As with other findings, this stromatolite case is not conclusive. As new isotopic techniques emerge, stromatolites
could be a focus of the convergence
of isotopic and morphological techniques for GOE research, according
to Konhauser. Bosak also hopes that
more unconventional lines of investigation, such as simulations that recreate ancient environments, will become
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an increasing part of the early-life
exploration.
Enter the GOE
Whereas most researchers now think
that cyanobacteria produced oxygen
before the GOE, the GOE remains
firmly established as a definite crossing 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 expansions 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 formations, which are ancient rocks that
indicate oxygen (or some other chemical that acts like oxygen) attaching
to Earth’s abundant iron (as happens
with rust). Red-banded iron formations 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 o
­ xidize all the things
in the environment around it, whether
it be reduced iron in the oceans, . . .
hydrogen gas coming out of volcanoes, . . . [or] methane produced
by. . . bacteria.” He adds, “There’s a
litany of different things. What the
GOE seems to represent is that tipping 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 formations 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 oxygenation, because they appear later in the
geological record. Moreover, the red
transformation can also be produced
from other geochemical (oxidizing)
processes without oxygen.
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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 preserved 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.
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 atmosphere. Farquhar’s research illustrated
that sulfur isotopes in the Earth’s early
atmosphere fractionate in a dependable way, but when oxygen is in the
atmosphere and there is consequently
an ozone layer, the fractionation disappears because the ozone blocks ultraviolet 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,
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with global carbon isotopic measurements indicating an oxygen rise to
perhaps 50 percent of current levels. Afterwards, according to Lyons’s
research, a deep drop in oxygen apparently 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 picture of a less potent atmosphere mixture 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, altering 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 lightest 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 volcanoes, their released gases, and carbon
burial are all associated with plate
tectonics and land formation, which
is an integral part of the early-oxygen
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investigation. “One of the most exciting 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 composition, I think that would be terrific.”
Rudnick points out that there are
a lot of uncertainties about continents, above-sea-level crust, volcanoes, 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 landmasses. 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 legacy
It is hard to overstate the impact of the
GOE on life on Earth. The researchers 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 environment and life is further underscored. “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 reactions on and just below the Earth’s
surface.
Not only do weathering and ecological niches formation take on new
forms, according to Konhauser, but
also the Earth is readied for the dominance 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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