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The Selfish Ribosome Theory Could Upend Evolution As We Know It

If it's true. But that's a big "if."
​A modern animal cell. Image: ​Wikipedia

When Aarhus University ecologist ​Meredith Root-Bernstein turned to her father and asked "What does DNA want?" the intent was not to question the majority of evolutionary theory. But to follow her question to its conclusion, the father-daughter team has been forced to do just that.

​Their theory is called the Selfish Ribosome, and it casts a familiar piece of modern cellular machinery as the central actor in early biological evolution. It's a seemingly small reorientation of evolutionary thinking, and if true, could give us a completely new understanding of the origin of life on Earth—but that's a big if.

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Our cells use ribosomes as tools today, but the Root-Bernsteins believe they have compelling evidence that at one point in our history, ribosomes may have ruled the world.

The Selfish Ribosome is a play on the title of Richard Dawkins' famous book The Selfish Gene, and the broad area of evolutionary theory it inspired. The central point of selfish gene theory is that evolution is driven primarily by the success or failure of genes, rather than the success or failure of the individual cells or animals that contain those genes.

The Root-Bernsteins also believe that there was a so-called selfish central actor at the beginning of evolution, a unit that drives evolutionary change solely according to its own survival and success, but they have a different candidate in mind: the ribosome.

Ribosomes are the gene-protein complexes that, in modern life, are responsible for translating a gene's code into its corresponding protein. Without the ribosome available to do that translation, a gene is unable to put its code into practice, as useless as an HTML file without a browser to interpret and express it.

The Selfish Ribosome theory argues that long before the onset of cellular life on Earth, ribosomes could have been simple replication robots. These non-living amalgamations of proteins and short genetic sequences would have been capable of making copies of their own features, and of the genes which encode those features. The protein machinery made new copies of genetic sequences, then used those new copies as blueprints to build another set of proteins just like itself.

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But there's a glaring hole in this plot: ribosomes themselves are made up of proteins. If ribosomes also make proteins, then what made the first ribosome? In a pre-biological, pre-evolutionary age, how could a ribosome have come to be so complex?

It's possible that each of the individual functions of a self-replicating ribosome might have been formed formed spontaneously from simpler molecules on ancient Earth.

That idea does naturally lend itself to a bit of experimentation. If a ribosome really did begin evolving as a singular unit, long before the development of cellular life, then its internal genetic material would have to have contained all blueprints needed to replicate those genes and build its own proteins—and that could be a testable hypothesis!

In their paper, the team shows that ribosomes in modern E. coli really do contain the disused vestiges of all the information they'd need if they could self-replicate. That doesn't prove their theory correct, but it is a hard requirement for it to be true.

"The ribosome seems to encode a lot of its own functions," said co-author and Michigan State University researcher Robert Root-Bernstein. "I don't think anybody expected that."

Still, even if it did exist at one point, a theoretical self-replicating ribosome was far from the end of biological development.

Eventually, some pre-living ribosomes would have associated with bubbles of fatty acids—the first cell membranes. At that point, it would have been advantageous to start collecting and fabricating a library of extra-ribosomal gene blueprints (a genome), since those free-floating protein products could now build up in concentration inside an enclosed space. Ribosomes that only translated their own internal genes into proteins didn't waste energy building proteins out of any old random sequence they happened to encounter, but they also couldn't reap the benefits of the occasional useful product.

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Over time, a ribosome's ability to compete with other ribosomes was dictated more and more strongly by the arsenal of genomic blueprints it had collected to strengthen the cell and supplement its own internal sequences. Eventually, ribosomes even used the genome to store the genes for their own ribosomal proteins, making them just another tool to be built and used by the genome, as needed.

Under this radically new view of the origin of life, genes only became independent of ribosomes because ribosomes began using them to gain an advantage over their rivals—while traditional theory says that ribosomes were only created and refined because they gave genes a more efficient way of affecting their surroundings and outcompeting their rivals.

This reorientation of early evolutionary theory around the success or failure of ribosomes, as opposed to the success or failure of genes, was the impetus for the metaphorical name, the Selfish Ribosome. A more accurate name might have been, The Ribosome as Origin of Evolution and Precursor of Life—but that wouldn't have been nearly as catchy.

Since now any gene in a cell could have access to that cell's ribosomal machinery, any gene could now affect the cell by having its code put into practice as a protein. Any change in such a gene would now also change the cell in which it resides, affecting that cell's ability to survive and replicate. This is the onset of classical cellular evolution—today, the genome unquestionably rules the cell, but seen through the lens of ribosome-first evolution, this may be a hijacking.

When the Selfish Ribosome was first published, one of the primary pieces of feedback surprised its creators. "We learned that [with E. coli] we'd used one of the worst organisms possible," said Root-Bernstein. He called E. coli a "worst case scenario" organism, since it has been subject to so much rapid evolution that its ribosomal sequences have likely greatly diverged from ancient versions. "We probably should have used some [more static organisms like] archaea or extremeophiles, since they'd probably have something much closer to their original ribosomes."

"That actually makes us feel better," he said. "If we can make our case in something like E. coli, then there are much better cases to be made with other organisms."

Obviously, their results aren't nearly strong enough to overturn close to a hundred years of theory on the origins of life, and so the plan is to search for more definitive results in better-suited organisms. Their findings could give us a better understanding of what DNA really wants, and whether a ribosome might have gotten there first.