Evolutionary biology: how complex life began on earth

One of the biggest puzzles in evolutionary biology is the emergence of complex living cells about 1.8 billion years ago. How did simple "prokaryotes" - small microbes which had monopolised terrestrial life for two billion years - become "eukaryotes", large cells with a complex internal structure that would later evolve into multicellular animals and plants?

Now a Swedish-Norwegian team has provided part of the answer, describing in the journal Nature a microbe that goes some way to bridging the gap between prokaryotes and eukaryotes. This "missing link", called Lokiarchaeota or Loki for short, lives 2.35km below the sea surface, at a hydrothermal vent between Greenland and Norway.

The researchers did not isolate or culture Loki as live microbes - they "reconstructed" it in virtual form from DNA extracted from seabed sediments around the hydrothermal vent. Genetic analysis shows that Loki has more biochemical features characteristic of eukaryotes than any other prokaryote discovered previously, including sophisticated enzymes and proteins involved in making cell membranes.

"We hoped that Loki would reveal a few more pieces of the puzzle but when we obtained the first results, we couldn't believe our eyes," says project leader Thijs Ettema of Uppsala University. "By studying its genome, we found that Loki represents an intermediate form in between the simple cells of microbes and the complex cell types of eukaryotes."

Soon after the first primitive self-replicating cells arose on earth about 3.8 billion years ago - by an unknown chemical process perhaps taking place around hydrothermal vents - life split into two broad prokaryotic groups, archaea and bacteria, which evolved separately. Loki is an archaeon.

Although Loki's features suggest that ancestral archaea had embarked on a path toward eukaryotic complexity, the key step took place later. An archaeon engulfed a bacterium and the two thrived together, united in a remarkable act of "endosymbiosis". In their descendants the former bacteria proliferated within the combined eukaryotic cell as energy-processing mitochondria, while most of the bacterial genes joined the archaeal DNA in a new cellular nucleus. The Scandinavian scientists argue that the pre-existing characteristics found in Loki would have facilitated a successful union.

Scientific exploration of the vast number of unknown microbes inhabiting extreme environments - sometimes referred to as "microbial dark matter" - is only just beginning with new genomics technology. "There is still a lot out there to discover and I am convinced that we will be forced to revise our biology textbooks more often in the near future," says Ettema.

Photograph: R.B. Pedersen, Centre for Geobiology, Bergen, Norway

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