Tree or ring: the origin of complex cells

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The natural world is full of great partnerships. Bacteria give animals the guts to digest all manner of otherwise inedible foods. Algae allow corals to harness the power of the sun and construct mighty reefs.  Ants cooperate to become mighty superorganisms. But the greatest partnership of all is far more ancient. It’s so old that we can only infer that it took place by looking for signals of history, embedded into the genomes of modern species. The details of how and when it happened are still the source of fierce debate but this was undoubtedly the most important merger in the history of life on Earth: a partnership between two simple cells that would underlie the rise of every living animal, plant, fungus and alga.

All complex life belongs to a single group called the eukaryotes, whose members, from humans to amoebas, share a common ancestry. Their cells are distinguished by having several internal compartments, including the nucleus, which shelters their precious DNA, and the mitochondria, which provide them with power.

This internal organisation sets the eukaryotes apart from the two other domains of life: the prolific bacteria; and the archaea, masters of extreme environments. These two groups are very different in their biochemistry but they are look superficially similar. Both are comprised of solitary cells that lack mitochondria or any other internal compartments; their DNA is unfettered by a nucleus. A chasm of organisation separates these simple cells from the complex eukaryotes, and the crossing of this chasm, several billion years ago, is one of the most important events in the planet’s history.

An event so deep in time was always going to be difficult to piece together. Those ancestral cells are hardly going to leave fossils behind, but there are clues to their ancient prehistory in the genomes of living species. Some genes are so important that they’re shared between all living things – neither bacterium nor human could do without them. These core genes have diverged over the course of evolution, but they’re similar enough to reflect a shared history. By comparing them across modern species, biologists can look at which are more closely related than others.

In the 1970s, the great biologist Carl Woese used one such gene to construct a grand tree of life, where eukaryotes and archaea are sister lineages, both descended from bacterial ancestors (left image above). This is the traditional view of the origin of eukaryotes, but it was based on just one gene. As others were analysed, a more confusing picture emerged. While many eukaryotic genes are indeed closely related to those of archaea, as predicted by Woese’s tree, others have more similar counterparts in bacteria.

These two classes also tend to have different roles. The archaea-like genes tend to be “informational” genes, which are involved in DNA: decoding it, using it to produce proteins, and making new copies of it. The bacteria-like genes tend to be “operational” – they’re involved in dogsbody jobs like making amino acids, fat molecules and so on.

Now, in a new study, James Cotton and James McInerney have found that the archaea-like genes also seem to be more important than the bacteria-like ones, even though they’re less common. The duo looked at every one of the 6,700 gene in the baker’s yeast Saccharomyces cerevisiae. They found that around 2,000 are most closely related to bacterial genes and just 500 or so are most closely related to archaeal ones.

But not all genes are equal. Some are so indispensible that if they don’t work, the yeast dies. And these vital genes are more than twice as likely to have archaeal counterparts as bacterial ones. There are other indicators of importance: the archaea-like genes are also about twice as active as the bacteria-like ones; they’re more likely to interact with other genes; and they’re present in fewer copies. So in the yeast genome, the archaea-like genes are a small group but an elite one.

Cotton and McInerney think that their results support a model for the origin of eukaryotes that’s very different to Woese’s tree. In this scenario – the so-called “ring of life” – eukaryotes arose from a fusion of the other two domains of life. In a fateful encounter, an archaeon swallowed a bacterium, setting up an alliance that would allow both of them to escape the restraints of their simple structures.

The bacterium was eventually domesticated, becoming the mitochondria of today. It transferred many of its genes into the host genome, producing the chimeric mash-up of archaeal and bacterial DNA that we see in modern eukaryotes. Meanwhile, it retained some of its own genes and indeed, mitochondria still have a small genome of their own.

Cotton and McInerney’s results certainly fit with this idea. The genes of the archaeal host have been interacting with each other for longer, well before any bacterial genes were added into the mix. Once that happened, some archaeal genes were displaced, but the essential few remained inviolate. Even after some 2 billion years of evolution, they’re still doing the same fundamental job. The bacterial additions had to be integrated around this core network. This explains why the archaea-like genes of yeast have a central importance out of all proportion to their small number.

That is not to say that the addition of the bacterium wasn’t a pivotal event. Nick Lane has written about this subject extensively in his beautiful book, Life Ascending, and cautions against over-interpreting the new study. “The impression might be created that the host cell was somehow ‘in charge’ all along and the mitochondria had a relatively minor, certainly less important, involvement in the evolution of the eukaryotic cell,” he says. “That would be totally wrong.”

“The host cell was utterly transformed by the mitochondria,” he says. “The fact that a few archaeal genes seem to be more important than bacterial genes should not distract from the fact that the eukaryotic cell is not an archaeon. It has transformed utterly and has thousands of new genes (even in yeast), none of which would have been possible without the mitochondria.”

Bill Martin, who also supports the ring of life model, thinks that it’s important that bacteria have “made a greater quantitative contribution to yeast (and eukaryote) genomes than archaea”. To him, this runs counter to the classical tree of life model, where archaea are the sisters to eukaryotes. It can only be explained by a “symbiotic origin of eukaryotes”, where archaea and bacteria both contributed to the origin of these complex cells.

Tom Cavalier-Smith, who still champions the tree of life model, sees things differently. To him, the archaea-like genes of yeast were simply those present in the last common ancestor of eukaryotes and archaea; they reflect the fact that the two groups are sisters. According to this view, the first eukaryotes had already evolved many of their complex features before they swallowed the bacterium that would eventually become mitochondria. The bacteria-like genes in yeast and other modern eukaryotes either come from these domesticated bacteria, or they’re slow-changing remnants of extremely ancient bacterial ancestors.

Cavalier-Smith also says that the new study doesn’t account for the fact that genes evolve at very different rates. Some of the most important genes that shaped the evolution of the early eukaryotes have changed so much that they can’t be ascribed to either archaea or bacteria. Those genes tell an important story, but they’re largely ignored by Cotton and McInerney.

And if there’s one thing that everyone agrees on, it’s that yeast genes are only part of the picture. For a start, yeast can survive without mitochondria. In eukaryotes that can’t, such as animals, Lane thinks that knocking out the bacterial genes would be far more costly. Martin agrees – he thinks that the “importance” of the archaeal hand-me-downs might vary from one species to another. “Time and more analyses will tell,” he says.

This is not a debate that’s going to be settled any time soon. Indeed, Woese emailed me simply to say that he didn’t want to get involved. Perhaps this is inevitable. The origin of eukaryotes – whether through the branching of a tree or the fusion of a ring – was a critical event that took place billions of years ago. Its singular importance makes it both endlessly fascinating and perhaps endlessly difficult to resolve.

Reference: PNAS http://dx.doi.org/10.1073/pnas.1000265107
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