If water is the key to life, then oxygen is the key to animal life. All animals breathe oxygen. Despite decades of research, however, scientists still don’t know when Earth’s atmosphere held enough free oxygen to support the planet’s early animals. Most geologists agree that oxygen first accumulated in the atmosphere around 2.4 billion years ago. But they don’t agree on how much there was at that time or if it was enough for animals to thrive.
My colleagues and I recently found new clues to help answer these questions from an unlikely source: the acidic, metal-rich waters of Rio Tinto in southern Spain. The composition of these waters is considered extreme today, yet the sort of acid rock drainage that causes these conditions was widespread long ago, when newly available atmospheric oxygen first began interacting with sulfur minerals on land.
In our work, we showed that the chemistry occurring in these acidic waters can reconcile seemingly contradictory estimates of past levels of breathable oxygen determined from ancient sediments. Our data support growing evidence that enough oxygen was present for animals to have evolved nearly 2 billion years before they burst onto the scene.
Earth’s First “Great Oxidation”
When the single-celled ancestors of plants learned to combine carbon dioxide and water, these early innovators spat out a waste product formerly absent from their environment: free molecular oxygen.
A critical transition in our planet’s history occurred when the single-celled ancestors of plants learned to combine carbon dioxide and water—two chemicals found everywhere on Earth—to make their cells and produce energy. These early innovators spat out a waste product formerly absent from their environment: free molecular oxygen (O2). This highly reactive gas began to run rampant on Earth’s surface, leaving telltale signs of its activity in minerals and sediments.
It’s been more than 5 decades since scientists began deciphering these signs from the geologic record. Over that time, most scientists have come to agree that O2 first reached appreciable concentrations in Earth’s atmosphere roughly 2.4 billion years ago, during the Great Oxidation Event (GOE) [Farquhar et al., 2014]. Geologists who first described the GOE estimated that oxygen levels rose from near zero to about 10%–40% of what they are today (oxygen currently makes up 21% of the air we breathe). They also proposed that atmospheric O2 remained at these levels until it reached modern levels more than 1.5 billion years later. This extended interval roughly coincided with the third and longest of the four geologic eons of Earth’s history, the Proterozoic.
Other researchers have since challenged those original estimates of Proterozoic O2. They suggest that oxygen concentrations rose to less than 0.1% of today’s level during the GOE and remained there, with only occasional short-term increases, through the ensuing eon. This substantial distinction—10% or more versus less than 0.1%—bears critically on the role of oxygen in animal evolution. Various forms of animal life require different minimum oxygen levels for survival, but even primitive animals like sponges require at least 0.25% of today’s atmospheric oxygen levels to metabolize [Cole et al., 2020].
In the fossil record, paleontologists have found the oldest undisputed fossil eukaryotes, the single-celled precursors to animals, in marine sediments that accumulated about 1.7 billion years ago [Knoll and Nowak, 2017]. Despite the undisputed antiquity of eukaryotes, fossils of large multicellular life-forms representing putative animals don’t appear until more than a billion years later in the 0.57-billion-year-old Ediacaran biota, and undisputed animals don’t appear until the Cambrian period about 0.54 billion years ago.
Paleontologists have also described a pronounced expansion of fossil eukaryotes around 0.8 billion years ago, coinciding with when atmospheric O2 reached near modern levels. Some researchers hypothesize that this rise in O2 allowed these early eukaryotes to diversify and eventually evolve into multicellular animals. But this simple cause-effect scenario relies heavily on debated claims that oxygen remained too low to sustain animal life for roughly 1.6 billion years prior.
Controversial Clues from Chromium
One problem with attempts to resolve the history of Earth’s breathable oxygen is that the data researchers use to estimate past levels have provided conflicting results.
One problem with attempts to resolve the history of Earth’s breathable oxygen is that the data researchers use to estimate past levels have provided conflicting results. The atmosphere doesn’t directly fossilize, so geochemists rely on indirect traces, or proxies, to tease out the gases it contained at different times.
One proxy that researchers have widely employed to estimate atmospheric O2 levels in the Proterozoic involves the heavy metal chromium [Wei et al., 2020]. Like many elements, not all chromium atoms are created equal. Although all have 24 protons in their nuclei, they can have different numbers of neutrons; in other words, different isotopes of chromium exist.
These different chromium isotopes react at different rates, leading to fractionation, or a change in their ratios, when they undergo chemical reactions in the environment. For example, chromium isotopes are fractionated when they react with manganese oxide minerals. This reaction preferentially releases heavier isotopes of chromium into natural waters that become more concentrated in sediments as a result.
Scientists want to resolve these disparate scenarios to understand oxygen’s role in animal evolution on Earth and potentially on other planets too.
Manganese oxide minerals such as birnessite and todorokite are very common in modern environments, for example, in soils and fluvial settings and on the seafloor. Researchers have estimated that reactions with these minerals fractionate chromium isotopes when free O2 is present at concentrations above 0.1% of modern atmospheric levels [Planavsky et al., 2014]. So some scientists have argued that chromium isotope fractionation in ancient rocks provides an “oxygen signal,” indicating when O2 exceeded 0.1% of current levels. They have also claimed the corollary, that a lack of chromium isotope fractionation in rocks indicates that oxygen levels at the time the rocks formed were below that threshold.
Geochemists who first measured chromium isotopes in Proterozoic rocks found that large chromium isotope fractionations didn’t appear until 0.8 billion years ago, suggesting O2 levels were too low to support animals until late in the Proterozoic [Planavsky et al., 2014]. However, researchers recently found large fractionations in chromium isotopes preserved in ancient soils and marine rocks as far back as 1.9 billion years ago. These researchers contended that Proterozoic O2 levels were at least intermittently high enough for animals to evolve well before their first occurrence in the fossil record [Canfield et al., 2018]. Scientists want to resolve these disparate scenarios to understand oxygen’s role in animal evolution on Earth and potentially on other planets too.
Going to the Extreme
Spain’s Rio Tinto flows roughly 100 kilometers through the southwest of the country, stained blood red from its headwaters north of the town of Nerva in the Sierra Moreno to its mouth at the Ria of Huelva estuary, where it spills into the Atlantic Ocean. Mining activities over millennia in the Iberian Pyrite Belt, one of the largest hydrothermal ore deposits in the world, have exposed large piles of the iron sulfide mineral pyrite in the headwaters of the river to attack by atmospheric O2 at Earth’s surface. When pyrite reacts with O2, it produces sulfuric acid, which is responsible for the river’s very low pH of 2 (similar to the pH of lemon juice or stomach acid). The reaction and resulting acidity also release iron, which gives rise to the river’s characteristic red tint, and other heavy metals—including chromium—from surrounding rocks.
Today, Rio Tinto’s waters are an extreme environment. But such conditions were once far more common. Scientists have proposed that as a result of the GOE, newly liberated O2 in the atmosphere attacked extensive pyrite deposits on the land surface. Like today’s rock weathering in southern Spain, this chemical attack released heavy metals and sulfuric acid, producing widespread acid rock drainage [Konhauser et al., 2011]. In the aftermath of the GOE, it’s likely that rivers like Rio Tinto were the norm rather than the exception.
Are scientists today similarly misinterpreting the lack of chromium isotope fractionation in rocks older than 0.8 billion years?
Despite the preponderance of acid rock drainage after the GOE, geochemists had not looked into how chromium isotopes fractionate in acidic natural waters. After nearly a decade of teaching geochemistry at Rio Tinto, I knew manganese oxides rarely form in similarly acidic waters. And I figured if manganese oxides are necessary for imparting the chromium isotopic oxygen signal into rocks, then a lack of these minerals might prevent the formation of the signal, even in today’s high-O2 atmosphere.
To investigate this hypothesis, I teamed up with my longtime friend and colleague Kate Scheiderich, who was then at the U.S. Geological Survey and had set up a lab to measure chromium isotopes. Returning to Rio Tinto, I collected samples of river water, rocks, and sediment from different locations along the bank of the river. Then I shipped them to Kate’s lab for her and another colleague to analyze.
We found that the acidic headwaters of the Rio Tinto were, indeed, leaching chromium from the surrounding rocks, then carrying it downstream to the Atlantic, where it accumulated in sediments around the estuary. However, the river was simply too acidic for manganese oxide minerals to form, despite flowing in an atmosphere with 21% oxygen. The analytical results in our study confirmed that without any manganese oxides to react with, chromium isotopes in the estuary sediments remained unfractionated and the chromium isotope values were identical to those in the source rocks they came from upstream (Figure 1).
Millions of years from now, after these estuarine sediments have lithified into marine rocks, future geochemists—analyzing the rocks with the same techniques and understanding of the chromium isotope oxygen signal scientists have employed until now—might thus mistakenly infer that our current air was unbreathable. Are scientists today similarly misinterpreting the lack of chromium isotope fractionation in rocks older than 0.8 billion years?
We proposed that the prevalence of acid rock drainage on Proterozoic continents could have hindered development of the chromium isotope oxygen signal until 0.8 billion years ago (when, perhaps, most acid rock drainage had been consumed). This idea reconciles seemingly contradictory chromium isotope data and suggests O2 in the atmosphere could have been elevated above 0.1% of modern levels far earlier in the Proterozoic [Scheiderich et al., 2023].
Why Did Animals Wait?
As scientists increasingly focus on oxygen in the Proterozoic, more geochemical estimates [e.g., Mänd et al., 2020] and atmospheric models [e.g., Gregory et al., 2021] are suggesting that atmospheric O2 concentrations were high enough for animals to have thrived more than 2 billion years before the early Cambrian. So why did it take so long for them to appear?
One possible explanation is that oxygen concentrations in the Proterozoic ocean fluctuated too much. Most scientists agree that shallow marine habitats, likely hotbeds for evolution, had oxygen levels high enough to support eukaryotes throughout the Proterozoic. But oxygen-free waters from the deep ocean routinely circulated upward, possibly diluting the oxygen oases at the surface. The instability of back-and-forth swings in oxygen in the surface ocean could have posed a big challenge to the evolution of early animals.
Some scientists suggest famine could also have held early animals back. The same protoplants that produced oxygen in the Proterozoic also formed the base of the food chain, so researchers have inferred that low oxygen and a low food supply went hand in hand. Animals could also have been starved for nutrients essential to life, such as nitrogen, which is found in nearly all biomolecules, including DNA, RNA, and proteins. Many geochemists have suggested nitrogen was scarce in the Proterozoic, when denitrifying microbes first started converting oxidized nitrogen (e.g., nitrate) into forms that animals can’t use (e.g., nitrogen gas).
Other researchers have proposed developmental hypotheses for the lag in animal evolution. They point out that it could have taken billions of years for the core set of genes found in all multicellular life to evolve in eukaryotes and that only after those genes emerged could animal life diversify greatly. Or perhaps, environmental and biological hurdles together slowed animal evolution.
For now, more answers to why animals only debuted at the end of the Proterozoic will have to wait. Whatever the explanations, recent research is seemingly making clear that it wasn’t for want of oxygen.
References
Canfield, D. E., et al. (2018), Highly fractionated chromium isotopes in Mesoproterozoic-aged shales and atmospheric oxygen, Nat. Commun., 9(1), 2871, https://doi.org/10.1038/s41467-018-05263-9.
Cole, D. B., et al. (2020), On the co‐evolution of surface oxygen levels and animals, Geobiology, 18(3), 260–281, https://doi.org/10.1111/gbi.12382.
Farquhar, J., A. L. Zerkle, and A. Bekker (2014), Geologic and geochemical constraints on Earth’s early atmosphere, in Treatise on Geochemistry, 2nd ed., pp. 91–138, Elsevier, Amsterdam, https://doi.org/10.1016/B978-0-08-095975-7.01304-8.
Gregory, B. S., M. W. Claire, and S. Rugheimer (2021), Photochemical modelling of atmospheric oxygen levels confirms two stable states, Earth Planet. Sci. Lett., 561, 116818, https://doi.org/10.1016/j.epsl.2021.116818.
Knoll, A. H., and M. A. Nowak (2017), The timetable of evolution, Sci. Adv., 3, e1603076, https://doi.org/10.1126/sciadv.1603076.
Konhauser, K. O., et al. (2011), Aerobic bacterial pyrite oxidation and acid rock drainage during the Great Oxidation Event, Nature, 478(7369), 369–373, https://doi.org/10.1038/nature10511.
Mänd, K., et al. (2020), Palaeoproterozoic oxygenated oceans following the Lomagundi–Jatuli event, Nat. Geosci., 13(4), 302–306, https://doi.org/10.1038/s41561-020-0558-5.
Planavsky, N. J., et al. (2014), Low mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals, Science, 346(6209), 635–638, https://doi.org/10.1126/science.1258410.
Scheiderich, K., A. L. Zerkle, and D. Damby (2023), Chromium isotopes in an acidic fluvial system: Implications for modern and ancient Cr isotope records, Geochim. Cosmochim. Acta, 354, 123–145, https://doi.org/10.1016/j.gca.2023.05.024.
Wei, W., et al. (2020), Biogeochemical cycle of chromium isotopes at the modern Earth’s surface and its applications as a paleo-environment proxy, Chem. Geol., 541, 119570, https://doi.org/10.1016/j.chemgeo.2020.119570.
Author Information
Aubrey Zerkle (aubrey.zerkle@bmsis.org), Blue Marble Space Institute of Science, Seattle, Wash.
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