The first organism to use oxygen may have appeared surprisingly early

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The first organisms to “breathe” oxygen—or at least use it—appeared 3.1 billion years ago, according to a new genetic analysis of dozens of families of microbes. The find is surprising because the Great Oxidation Event, which filled Earth’s atmosphere with the precious gas, didn’t occur until some 500 million years later.

“I was pretty thrilled to see this paper,” says Patrick Shih, an evolutionary biologist at the University of California (UC), Davis. The advent of proteins that can use oxygen, Shih and others say, marks a key step in the emergence of aerobic microbes, which are those able to harness oxygen. “The transition from a world that was mostly anaerobic to one that was mostly aerobic was one of the major innovations in life,” says Tim Lyons, a biogeochemist at UC Riverside.

Scientists broadly agree that Earth’s early atmosphere and oceans were all but devoid of oxygen gas. But there are signs that there was some oxygen around. Geochemists, for example, have found mineral deposits dated to about 3 billion years ago that they argue could only have formed in the presence of oxygen. And some evidence suggests cyanobacteria, the earliest photosynthetic organisms to release oxygen gas as a waste product—although not use it—may have arisen as early as 3.5 billion years ago.

Yet critics have countered that if oxygen producers and users came along that early, they would have spread quickly across the globe. That’s because using oxygen allows organisms to harness more energy from their food. But the Great Oxidation Event didn’t occur until 2.4 billion years ago.

In the new study, Dan Tawfik, a biological chemist at the Weizmann Institute of Science, and his Ph.D. student Jagoda Jabłońska, decided to come at the problem from a different direction. They analyzed the genomes of 130 families of prokaryotes, the living descendants of what are considered Earth’s earliest microbes, bacteria, and archaea. Tawfik and Jabłońska created an evolutionary family tree using the genes for some 700 enzymes that either use or generate oxygen. Then, they turned to a long-used approach that tracks the likely mutation rate of proteins to construct a “molecular clock.” The clock enabled them to pin down when each of these enzymes likely evolved. Of the 130 families of organisms they studied, Jabłońska and Tawfik were able to date 36 with high confidence.

“We saw something quite striking,” Tawfik says: a “clear burst” of microbes using oxygen between 3 billion and 3.1 billion years ago. Twenty-two of the 36 families appear to have emerged at that time, while 12 came later, and only two seemed to come before, the team reports today in Nature Ecology & Evolution.

Overall, the analysis suggests that about 3.1 billion years ago, an organism they dub the last universal oxygen ancestor emerged, Tawfik says. That ancestor in turn gave rise to aerobes that were able to take advantage of the increased energy output that oxygen use enabled. Eventually, this led to multicellular organisms, animals, and us.

If that transition did occur about 3 billion years ago, it suggests oxygen-using organisms didn’t immediately sweep across the planet. Rather, the ability to use oxygen likely evolved in small pockets that slowly spread over hundreds of millions of years. And only when they became abundant enough did these organisms modify Earth’s environment enough to produce enough oxygen to lead to the Great Oxidation Event. “I feel like an archaeologist that is opening a grave for the first time,” Tawfik says.

Still, Shih and others caution that molecular clock dating is still an evolving science, and thus the team’s dating could be off. “The order of events is almost certainly robust,” says Roger Buick, an astrobiologist at the University of Washington, Seattle. “But the timing of the events may not be.”

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