Early Life Forms May Have Used Oxygen Pre-Atmosphere

Massachusetts Institute of Technology

Oxygen is a vital and constant presence on Earth today. But that hasn't always been the case. It wasn't until around 2.3 billion years ago that oxygen became a permanent fixture in the atmosphere, during a pivotal period known as the Great Oxidation Event (GOE), which set the evolutionary course for oxygen-breathing life as we know it today.

A new study by MIT researchers suggests some early forms of life may have evolved the ability to use oxygen hundreds of millions of years before the GOE. The findings may represent some of the earliest evidence of aerobic respiration on Earth.

In a study appearing today in the journal Palaeogeography, Palaeoclimatology, Palaeoecology , MIT geobiologists traced the evolutionary origins of a key enzyme that enables organisms to use oxygen. The enzyme is found in the vast majority of aerobic, oxygen-breathing life forms today. The team discovered that this enzyme evolved during the Mesoarchean - a geological period that predates the Great Oxidation Event by hundreds of millions of years.

The team's results may help to explain a longstanding puzzle in Earth's history: Why did it take so long for oxygen to build up in the atmosphere?

The very first producers of oxygen on the planet were cyanobacteria - microbes that evolved the ability to use sunlight and water to photosynthesize, releasing oxygen as a byproduct. Scientists have determined that cyanobacteria emerged around 2.9 billion years ago. The microbes, then, were presumably churning out oxygen for hundreds of millions of years before the Great Oxidation Event. So, where did all of cyanobacteria's early oxygen go?

Scientists suspect that rocks may have drawn down a large portion of oxygen early on, through various geochemical reactions. The MIT team's new study now suggests that biology may have also played a role.

The researchers found that some organisms may have evolved the enzyme to use oxygen hundreds of millions of years before the Great Oxidation Event. This enzyme may have enabled the organisms living near cyanobacteria to gobble up any small amounts of oxygen that the microbes produced, in turn delaying oxygen's accumulation in the atmosphere for hundreds of millions of years.

"This does dramatically change the story of aerobic respiration," says study co-author Fatima Husain, a postdoc in MIT's Department of Earth, Atmospheric and Planetary Sciences (EAPS). "Our study adds to this very recently emerging story that life may have used oxygen much earlier than previously thought. It shows us how incredibly innovative life is at all periods in Earth's history."

The study's other co-authors include Gregory Fournier, associate professor of geobiology at MIT, along with Haitao Shang and Stilianos Louca of the University of Oregon.

First respirers

The new study adds to a long line of work at MIT aiming to piece together oxygen's history on Earth. This body of research has helped to pin down the timing of the Great Oxidation Event as well as the first evidence of oxygen-producing cyanobacteria . The overall understanding that has emerged is that oxygen was first produced by cyanobacteria around 2.9 billion years ago, while the Great Oxidation Event - when oxygen finally accumulated enough to persist in the atmosphere - took place much later, around 2.33 billion years ago.

For Husain and her colleagues, this apparent delay between oxygen's first production and its eventual persistence inspired a question.

"We know that the microorganisms that produce oxygen were around well before the Great Oxidation Event," Husain says. "So it was natural to ask, was there any life around at that time that could have been capable of using that oxygen for aerobic respiration?"

If there were in fact some life forms that were using oxygen, even in small amounts, they might have played a role in keeping oxygen from building up in the atmosphere, at least for a while.

To investigate this possibility, the MIT team looked to heme-copper oxygen reductases, which are a set of enzymes that are essential for aerobic respiration. The enzymes act to reduce oxygen to water, and they are found in the majority of aerobic, oxygen-breathing organism today, from bacteria to humans.

"We targeted the core of this enzyme for our analyses because that's where the reaction with oxygen is actually taking place," Husain explains.

Tree dates

The team aimed to trace the enzyme's evolution backward in time to see when the enzyme first emerged to enable organisms to use oxygen. They first identified the enzyme's genetic sequence and then used an automated search tool to look for this same sequence in databases containing the genomes of millions of different species of organisms.

"The hardest part of this work was that we had too much data," Fournier says. "This enzyme is just everywhere and is present in most modern living organism. So we had to sample and filter the data down to a dataset that was representative of the diversity of modern life and also small enough to do computation with, which is not trivial."

The team ultimately isolated the enzyme's sequence from several thousand modern species and mapped these sequences onto an evolutionary tree of life, based on what scientists know about when each respective species has likely evolved and branched off. They then looked through this tree for specific species that might offer related information about their origins.

If, for instance, there is a fossil record for a particular organism on the tree, that record would include an estimate of when that organism appeared on Earth. The team would use that fossil's age to "pin" a date to that organism on the tree. In a similar way, they could place pins across the tree to effectively tighten their estimates for when in time the enzyme evolved from one species to the next.

In the end, the researchers were able to trace the enzyme as far back as the Mesoarchean - a geological era that lasted from 3.2 to 2.8 billion years ago. It's around this time that the team suspects the enzyme - and organisms' ability to use oxygen - first emerged. This period predates the Great Oxidation Event by several hundred million years.

The new findings suggest that, shortly after cyanobacteria evolved the ability to produce oxygen, other living things evolved the enzyme to use that oxygen. Any such organism that happened to live near cyanobacteria would have been able to quickly take up the oxygen that the bacteria churned out. These early aerobic organisms may have then played some role in preventing oxygen from escaping to the atmosphere, delaying its accumulation for hundreds of millions of years.

"Considered all together, MIT research has filled in the gaps in our knowledge of how Earth's oxygenation proceeded," Husain says. "The puzzle pieces are fitting together and really underscore how life was able to diversify and live in this new, oxygenated world."

This research was supported, in part, by the Research Corporation for Science Advancement Scialog program.

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