Mystery Microorganism May Have Been the First to Produce Oxygen

(Inside Science) -- One of the most pivotal moments in Earth's history was the evolution of the photosynthetic life that suffused air with the oxygen on which virtually all complex life on the planet now depends. Now the mystery of how that moment happened is deepening: Scientists have found that the genes for such photosynthesis apparently came from a now-extinct mystery source.

Although oxygen currently makes up about one-fifth of Earth's air, early in the planet's history, there was at least 100,000 times less atmospheric oxygen. Oxygen easily reacts with other molecules, and as such readily gets pulled from the atmosphere.

It was only with what is known as the Great Oxidation Event, roughly 2.3 billion years ago, that the element began accumulating in the Earth's primordial atmosphere to any major extent. This rise in oxygen stimulated the evolution of oxygen-breathing life, which in turn spurred the origins of the complex multicellular organisms that dominate the world now.

Prior research suggested this rise in oxygen levels was likely due to cyanobacteria -- so-called "blue-green algae" that generally are photosynthetic like plants, harvesting energy from the sun. Whereas simpler, more primitive "anoxygenic" forms of photosynthesis do not generate oxygen, cyanobacteria are unique among known bacteria for practicing the more complex process of oxygenic photosynthesis, which does generate the gas.

Oxygenic photosynthesis has come to dominate the globe in part because it generates two to three times more energy per photon of light than anoxygenic versions, said study co-author Woodward Fischer, a geobiologist at the California Institute of Technology in Pasadena. In addition, whereas anoxygenic photosynthesis requires materials such as hydrogen sulfide as sources of electrons for their chemical reactions, oxygenic photosynthesis only needs water, which is far more abundant on Earth's surface. All in all, oxygenic photosynthesis "ramped up the energetics of the biosphere to 11," Fischer said.

However, much remains unknown about when and how cyanobacteria evolved oxygenic photosynthesis. "The whole question of the origin of cyanobacteria has long been a mystery because they kind of just appeared out of the tree of life with this very advanced capability to do oxygenic photosynthesis without any apparent forebears," said biochemist Robert Blankenship at Washington University in St. Louis, Missouri.

Until recently, all known cyanobacteria were photosynthetic members of class Oxyphotobacteria.

But in 2013, researchers discovered a nonphotosynthetic class of cyanobacteria known as Melainabacteria. Now Fischer and his colleagues have discovered a second class of nonphotosynthetic cyanobacteria, the Sericytochromatia. The researchers suggest that both groups are clearly closely related to photosynthetic cyanobacteria, based on their genomes, but the two groups do not perform photosynthesis themselves.

One possible explanation for the lack of photosynthesis in these two classes of cyanobacteria was that they could once photosynthesize but then lost the ability. To find out more about this critical question, Fischer and his colleagues analyzed the genomes of 41 different kinds of nonphotosynthetic cyanobacteria. The team's analysis of 38 Melainabacteria genomes and three Sericytochromatia genomes found no trace of photosynthetic machinery.

"This pretty strongly suggests that the ancestor of all three lineages of cyanobacteria was not photosynthetic," said Blankenship, who did not take part in this research.

The fact that Oxyphotobacteria possess the complex apparatus for oxygenic photosynthesis while their closest relatives do not suggests that Oxyphotobacteria may have imported the genes for photosynthesis from another organism via a process known as lateral gene transfer. It remains a mystery what the source of these genes was, "and because it happened long ago, it's pretty likely that the group may actually have gone extinct," Fischer said.

Current cyanobacteria also "consume" oxygen, and the researchers found that the three classes of cyanobacteria use very different proteins to respire the gas, suggesting they likely acquired this cellular machinery independently from each other. The new finding suggests that today's groups evolved such respiration after the development of oxygenic photosynthesis.

Recent estimates suggest that Oxyphotobacteria diverged from their nonphotosynthetic brethren about 2.5 billion to 2.6 billion years ago. This strengthens the idea that the Great Oxidation Event about 2.3 billion years ago was caused directly by the evolution of oxygenic photosynthesis.

"It took a substantial unfolding of evolutionary time before oxygenic photosynthesis developed, perhaps because, as we know, it was a very challenging biochemistry to develop," Fischer said. "In this case, we had to wait until somewhere near the halfway point in our planet's history."

Future research can look for "missing links" that bridge the gap from anoxygenic photosynthesis to oxygenic photosynthesis. "They may all be gone done, but there are still a lot of undiscovered organisms out there in the environment, and it's tremendously important to keep looking for them," Blankenship said.

The scientists detailed their findings in the March 31 issue of the journal Science.