The search is on for Earth's missing two billion years

2.5 billion years ago, some highly-efficient bacteria began what's known as the oxygen revolution. 600 million years ago, the first multicellular animals appeared. What happened in between? We're really not sure - but geologists are working on it.

Here's the quick version of Earth's 4.54 billion year history. When the Earth first formed, the atmosphere was a mix of nitrogen and its oxides, carbon dioxide, methane, ammonia, sulfur dioxide, and hydrogen sulfide. Needless to say, modern humans (or any other form of life that depends on oxygen to survive) wouldn't last long on such a world. Oceans formed out of a mix of condensing water vapor and icy comet impacts, and these ancient oceans became vast reservoirs of dissolved iron, which was brought into the ocean through hydrothermal vents.

This was more or less the status quo for nearly two billion years. Simple lifeforms that could survive on this inhospitable mix of gases emerged, though none were bigger than a single cell. Despite their small stature, one of these first organisms set in motion a process that would change everything. These were the cyanobacteria (also known as blue-green algae), remarkably self-sufficient creatures that could both photosynthesize energy and oxygen from sunlight, and fix nitrogen, a process where nitrogen gas is converted into ammonia.

The search is on for Earth's missing two billion years

It's the first of those two process that is important here, because their photosynthesizing started releasing steady amounts of oxygen into the atmosphere. The oxygen levels skyrocketed 2.5 billion years ago, taking its modern place as a major part of the atmosphere and enabling the rise of aerobic lifeforms, or organisms that use oxygen to power their metabolism. This is known as the Great Oxygenation Event, and it also set the stage for more complex forms of life that could be larger than a single cell.

And then...nothing happened. At least, not for another two billion years. It wouldn't be until about 600 million years ago, during the Ediacaran Period, that the first multicellular organisms finally emerged. So what happened during that immense, multi-billion year gap? Why did it take so long for more complex life to arrive on the scene? For that matter, why did oxygen suddenly spike 2.5 billion years ago?

The simple, uncomfortable answer is that we don't really know. Geologists have gleaned a few crucial details about this long ago world in the last decade or so. Don Canfield, a geologist at Denmark's Odense University, complicated the picture in 1998 when he suggested sulfur compounds were also a vital part of the transformation of the Earth.

He argued that the old story, which held that the newly-freed oxygen had caused iron to dissolve out of the ancient oceans, was incomplete. In its place, he suggested that early oxygen-related erosion of rocks had released sulfates, which are ionic compounds of sulfuric acid. Bacteria in the ocean took these sulfates and converted them into sulfides, keeping the oxygen released from the the sulfates and leaving the now negatively-charged sulfur ions behind.

The search is on for Earth's missing two billion years

These sulfide ions bonded with the iron dissolved in the ocean, creating iron sulfide minerals like pyrite that solidified and dropped out of their dissolved form in the ocean. Even so, there were still plenty of toxic sulfide particles left over, and it took two billion years for bacteria to produce enough oxygen to remove them from the ocean depths. Then, and only then, could more complex life emerge.

It's a persuasive theory, but we simply don't have enough data to prove or disprove it, and all these theories make a basic, potentially flawed assumption. They all presume these processes were uniform all over the planet, when the latest data suggests the ancient world was anything but homogeneous.

David Fike, a geochemist at Washington University in St. Louis, outlines the challenges his scientific community will have to overcome to find the answers they seek:

"Recent geochemical evidence indicates that, at least locally, ferruginous (iron rich) or even sulphidic (sulfur rich) conditions persisted through the Ediacaran period, long after the Great Oxygenation Event. Things are much more complicated than we had supposed. As a community, we don't have a good sense of the spatial variation of these zones within different bodies of water. What's more, different assessments can arise from the interpretation of different geochemical proxies, from physical separation between different ocean basins, or from the reworking of sediments after deposition. As we try to unravel these changes in Earth's history, we often don't have 100 different places where we can measure rocks of the same age. We're stuck with a few samples, and the natural tendency is to take your rocks and extrapolate."

Fike argues the only way out of this mess is to get more data. To do that, geologists need redox proxies, which are isotope ratios in ancient rock formations that can help us extrapolate the nature of the Earth's ancient atmosphere and whether oxygen levels were increasing or reducing in a given time period. And, as increasingly appears to be the case, in a given spatial location. With enough redox proxies in place, we can put together a properly robust model of the ancient world that has clear detail in both the temporal and spatial directions, and will allow us to move past the rather flimsy collection of assumptions we're currently forced to make.

The search is on for Earth's missing two billion years

To illustrate how a lack of data can lead geologists astray, Fike points to the case of some spiny microfossils found in the Doushantuo formation in southern China. These tiny fossils, known as acritarchs, were thought to either be green algae or a kind of anaerobic plankton. Because the algae explanation seemed to fit with the current theories, that's what the scientists pursued, and as Fike explains, that's where they made their mistake:

"Scientists looking at the Doushantuo thought they understood what they were seeing," Fike says. "Oxygen is appearing, the acritarchs are evolving, and this is the start of the big rise in evolution associated with the final oxygen event. But then they noticed that after the big rise in spiny cysts and just when we see evidence for oxygen in the rock record, the acritarchs disappear. And that really doesn't make sense if you're evolving new groups because of the increase in oxygen. In 2009 a group of scientists led by Phoebe Cohen of Harvard University inspected acritarchs with transmission electron microscopes and concluded that they are not algae but rather animals, encased in protective cysts that animals form when conditions are not favorable to life."

These findings were later confirmed when a team of scientists (including Fike) went back to Doushantuo and took more redox proxy measurements. These revealed the ancient waters were rich in iron and sulfur, both of which would have killed any oxygen-dependent species.

As Fike is quick to point out, there's a lot more work ahead for geochemists. Although he believes adding greater spatial complexity will ultimately bring clarity to their models of the ancient atmosphere, they will also have to be more careful about misleading data caused by sediments that shifted in the last two billion years. Still, even if the puzzle is still far from complete, at least geologists have a better sense of how big it needs to be. The search continues for Earth's lost youth - all two billion years of it.

[Nature Geoscience; images are an artist's conception of the primordial Earth, cyanobacteria, bubbles in the ocean, and an acritarch.]