CHAMPAIGN, Ill. — Life did not begin with one primordial cell. Instead, there were initially at least three simple types of loosely constructed cellular organizations. They swam in a pool of genes, evolving in a communal way that aided one another in bootstrapping into the three distinct types of cells by sharing their evolutionary inventions. The driving force in evolving cellular life on Earth, says Carl Woese, a microbiologist at the University of Illinois at Urbana-Champaign, has been horizontal gene transfer, in which the acquisition of alien cellular components, including genes and proteins, work to promote the evolution of recipient cellular entities.
Woese presents his theory of cellular evolution, which challenges long-held traditions and beliefs of biologists, in the June 18 issue of the Proceedings of the National Academy of Sciences.
Cellular evolution, he argues, began in a communal environment in which the loosely organized cells took shape through extensive horizontal gene transfer. Such a transfer previously had been recognized as having a minor role in evolution, but the arrival of microbial genomics, Woese says, is shedding a more accurate light. Horizontal gene transfer, he argues, has the capacity to rework entire genomes. With simple primitive entities this process can "completely erase an organismal genealogical trace."
His theory challenges the longstanding Darwinian assumption known as the Doctrine of Common Descent – that all life on Earth has descended from one original primordial form.
"We cannot expect to explain cellular evolution if we stay locked in the classical Darwinian mode of thinking," Woese said. "The time has come for biology to go beyond the Doctrine of Common Descent."
"Neither it nor any variation of it can capture the tenor, the dynamic, the essence of the evolutionary process that spawned cellular organization," Woese wrote in his paper.
Going against traditional thinking is not new to Woese, a recipient of the National Medal of Science (2000), and holder of the Stanley O. Ikenberry Endowed Chair at Illinois.
In the late 1970s Woese identified the Archaea, a group of microorganisms that thrive primarily in extremely harsh environments, as a separate life form from the planet's two long-accepted lines – the typical bacteria and the eukaryotes (creatures like animals, plants, fungi and certain unicellular organisms, whose cells have a visible nucleus). His discovery eventually led to a revision of biology books around the world.
The three primary divisions of life now comprise the familiar bacteria and eukaryotes, along with the Archaea. Woese argues that these three life forms evolved separately but exchanged genes, which he refers to as inventions, along the way. He rejects the widely held notion that endosymbiosis (which led to chloroplasts and mitochondria) was the driving force in the evolution of the eukaryotic cell itself or that it was a determining factor in cellular evolution, because that approach assumes a beginning with fully evolved cells.
His theory follows years of analysis of the Archaea and a comparison with bacterial and eukaryote cell lines.
"The individual cell designs that evolved in this way are nevertheless fundamentally distinct, because the initial conditions in each case are somewhat different," Woese wrote in his introduction. "As a cell design becomes more complex and interconnected a critical point is reached where a more integrated cellular organization emerges, and vertically generated novelty can and does assume greater importance."
Woese calls this critical point in a cell's evolutionary course the Darwinian Threshold, a time when a genealogical trail, or the origin of a species, begins. From this point forward, only relatively minor changes can occur in the evolution of the organization of a given type of cell.
To understand cellular evolution, one must go back beyond the Darwinian Threshold, Woese said.
His argument is built around evidence "from the three main cellular information processing systems" – translation, transcription and replication – and he suggests that cellular evolution progressed in that order, with translation leading the way.
The pivotal development in the evolution of modern protein-based cells, Woese said, was the invention of symbolic representation on the molecular level – that is, the capacity to "translate" nucleic acid sequence into amino acid sequence.
Human language is another example of the evolutionary potential of symbolic representation, he argues. "It has set Homo sapiens entirely apart from its (otherwise very close) primitive relatives, and it is bringing forth a new level of biological organization," Woese wrote.
The advent of translation, he said, caused various archaic nucleic-based entities to begin changing into proteinaceous ones, emerging as forerunners of modern cells as genes and other individual components were exchanged among them. The three modern types of cellular organization represent a mosaic of relationships: In some ways one pair of them will appear highly similar; in others a different pair will.
This, Woese said, is exactly what would be expected had they individually begun as distinct entities, but during their subsequent evolutions they had engaged in genetic cross-talk – they had indulged in a commerce of genes.
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