Feature: Shaking the tree of life

2 October 2006. By Henry Nicholls, a freelance science journalist

Once, we thought the relationships between all living things - the branches of the tree of life - were straightforward and simple. Genetics is showing how wrong we were.

In the beginning there were the prokaryotes, simple cells such as bacteria. Eventually, these gave rise to the eukaryotes, more complex cells boasting a distinct nucleus and prokaryote-like internal structures such as mitochondria and chloroplasts. At least, that's the textbook version of how life on Earth unfolded. Sadly, it's completely wrong.

The multitude of genetic sequences that have been gathered from all manner of species suggest that this simple account is in need of a serious rewrite. The tree of life - a description of the evolutionary relationships among the myriad of organisms that make up life on Earth - looks far more complex than previously imagined.

The proposition that all living things are the products of descent (with modification) from common ancestors goes back to Ernst Haeckel, one of the most vocal early supporters of Charles Darwin's ideas on evolution. If evolution is a reality, Haeckel reasoned, then all living things (and for that matter all things that had ever lived) could be placed on a branching tree.

This ultimately gave rise to the neat, bifurcating tree that has become entrenched in our textbooks: a tree rooted in the prokaryotes, with a significant cellular innovation resulting in the eukaryotes.

Genetic roots

The ability to sequence genetic material from the late 1970s onwards marked a huge change for those trying to describe the tree of life. No longer did they have to rely on morphology (the shapes and structures of cells and organisms) alone. With genetic sequences to compare and contrast, they now had a new tool that reflected the evolutionary process.

The small subunit of ribosomal RNA (rRNA) is particularly useful for this kind of molecular inspection, as it is required by all living organisms to make proteins. The ubiquity of this 'universal molecular chronometer' strongly supports the assumption that life evolved just once, and its slow rate of evolution makes it useful for teasing apart some of the earliest evolutionary events.

One of the first revelations rRNA comparison threw up was that there were not two but three main branches to the tree of life. The archaea, identified by microbiologist Carl Woese in 1977, lacked a membrane-bound nucleus and therefore looked a lot like bacteria. But, in fact, they are more closely related to eukaryotes. This made a nonsense of the conventional story that prokaryotes evolved into eukaryotes.

In general, studies of DNA sequences from other genes confirm the three main branches suggested by inspection of rRNA. But they also reveal so much detail that the simple tree becomes far more complex and, in fact, less like a tree. In particular, the molecular genetic approach has resulted in a deluge of previously undescribed taxa that need to be accommodated. Among bacteria, for example, there are now more than 50 phyla (subdivisions of the prokaryotic kingdom) that can be reliably distinguished on the basis of their DNA. And these known groups probably only account for a fraction of the bacterial biodiversity waiting to be described. Excitingly, the relatively little-known archaea also turn out to be far more diverse than initially supposed. When Woese identified this branch in the late 1970s, they had only been found living in extreme environments such as hot springs. There is now molecular evidence that places these poorly understood organisms in just about every ecological niche on Earth.

A complex web

The tree gets more complex still. The mass sequencing of whole communities of bacteria, such as in the gut or in soil, has shown that many are adept at exchanging genetic material, often from one phylum to another. This process, known as horizontal gene transfer, means there's a real risk of interpreting a genetic similarity between two species as a close evolutionary relationship. Thankfully, it looks as though there are several genes that rarely undergo horizontal gene transfer; these could be used to help untangle the complex evolutionary history of this vast group of organisms.

This means that although a tree is still useful for illustrating such evolutionary relationships, many of its twigs and branches are somehow linked. To stick with the analogy, we should really imagine this domain of the tree laced with horizontal threads spun by a lively spider. There is even evidence that such horizontal gene transfer may have occurred in other domains of the tree. There are bits of the human genome, for example, that seem to have come from archaea, and others apparently from bacteria. Whether this can be explained by horizontal gene transfer or not, there are clearly vast areas of the tree of life that need to be clarified.

One such area is at the base of the eukaryote branch that grew into animals, plants, fungi and protists (which include protozoa and most algae). Understandably, there is considerable interest in pinning down the evolution of the cellular complexity that gave rise to multicellularity and ultimately to Homo sapiens. The rRNA tree suggested a compelling account: there were primitive eukaryotes, the so-called archezoa, that had a nucleus but no mitochondria; these early eukaryotes, the first trees implied, bridged the gulf between prokaryotes and full-blown, organelle-rich eukaryotes.

But this version of events is too good to be true. Membrane-bound structures present in the so-called archezoa carry molecular clues indicating that they are descended from mitochondria rather than primitive precursors to them. This has left a lot of unknowns at the base of the eukaryote branch of the tree.

Even within the eukaryotes, closer scrutiny of a wider array of genes is producing plenty of surprises. The nematode worm Caenorhabditis elegans, for example, looks like a simple beast. It has no legs, no body cavity and its rRNA signature suggests it is rather primitive, somewhere near the base of the eukaryote branch. But inspection of other genes reveals that its ancestors were complex, possibly even segmented. To pursue the tree metaphor, the nematode's molecular make-up indicates that branches don't always grow up but can turn downwards, giving organisms the illusion of being primitive when, in fact, they are simplifications of ancestral complexity.

As researchers continue to refine the tree of life, further twists and turns of its branches will surely be revealed. And why does all this matter? Mark Blaxter, Professor of Evolutionary Genomics at the University of Edinburgh in Scotland, offers two-and-a-half-answers.

The first is biomedical. If we want to use organisms such as flies and worms to model human disease, it's important to understand their relationships to us and to each other. This puts limits on our speculation about what such creatures can teach us, he says. Professor Blaxter's second answer is about biodiversity: "Until we know what we're killing off, our attempts at conserving biodiversity are probably mistaken." And the half answer? "Because it's absolutely fascinating."

Image credit: iStockphoto

Further reading

• Baum DA et al. Evolution. The tree-thinking challenge. Science 2005;310(5750):979-80.
• Embley TM, Martin W. Eukaryotic evolution, changes and challenges. Nature 2006;440(7084):623-30.
• Pace NR. Time for a change. Nature 2006;441(7091):289.
• Robertson CE et al. Phylogenetic diversity and ecology of environmental Archaea. Curr Opin Microbiol 2005;8(6):638-42.