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Thursday, 1 December 2011

Life began with a planetary mega-organism

ONCE upon a time, 3 billion years ago, there lived a single organism called LUCA. It was enormous: a mega-organism like none seen since, it filled the planet's oceans before splitting into three and giving birth to the ancestors of all living things on Earth today.

This strange picture is emerging from efforts to pin down the last universal common ancestor - not the first life that emerged on Earth but the life form that gave rise to all others.

The latest results suggest LUCA was the result of early life's fight to survive, attempts at which turned the ocean into a global genetic swap shop for hundreds of millions of years. Cells struggling to survive on their own exchanged useful parts with each other without competition - effectively creating a global mega-organism.

It was around 2.9 billion years ago that LUCA split into the three domains of life: the single-celled bacteria and archaea, and the more complex eukaryotes that gave rise to animals and plants (see timeline). It's hard to know what happened before the split. Hardly any fossil evidence remains from this time, and any genes that date that far back are likely to have mutated beyond recognition.

That isn't an insuperable obstacle to painting LUCA's portrait, says Gustavo Caetano-Anollés of the University of Illinois at Urbana-Champaign. While the sequence of genes changes quickly, the three-dimensional structure of the proteins they code for is more resistant to the test of time. So if all organisms today make a protein with the same overall structure, he says, it's a good bet that the structure was present in LUCA. He calls such structures living fossils, and points out that since the function of a protein is highly dependent on its structure, they could tell us what LUCA could do.

"Structure is known to be conserved when sequences aren't," agrees Anthony Poole of the University of Canterbury in Christchurch, New Zealand, though he cautions that two very similar structures could conceivably have evolved independently after LUCA.

To reconstruct the set of proteins LUCA could make, Caetano-Anollés searched a database of proteins from 420 modern organisms, looking for structures that were common to all. Of the structures he found, just 5 to 11 per cent were universal, meaning they were conserved enough to have originated in LUCA (BMC Evolutionary Biology, DOI: 10.1186/1471-2148-11-140).

By looking at their function, he concludes that LUCA had enzymes to break down and extract energy from nutrients, and some protein-making equipment, but it lacked the enzymes for making and reading DNA molecules.

This is in line with unpublished work by Wolfgang Nitschke of the Mediterranean Institute of Microbiology in Marseille, France. He reconstructed the history of enzymes crucial to metabolism and found that LUCA could use both nitrate and carbon as energy sources. Nitschke presented his work at the UCL Symposium on the Origin of Life in London on 11 November.

If LUCA was made of cells it must have had membranes, and Armen Mulkidjanian of the University of Osnabrück in Germany thinks he knows what kind. He traced the history of membrane proteins and concluded that LUCA could only make simple isoprenoid membranes, which were leaky compared with more modern designs (Proceedings of the International Moscow Conference on Computational Molecular Biology, 2011, p 92).

LUCA probably also had an organelle, a cell compartment with a specific function. Organelles were thought to be the preserve of eukaryotes, but in 2003 researchers found an organelle called the acidocalcisome in bacteria. Caetano-Anollés has now found that tiny granules in some archaea are also acidocalcisomes, or at least their precursors. That means acidocalcisomes are found in all three domains of life, and date back to LUCA (Biology Direct, DOI: 10.1186/1745-6150-6-50).

So LUCA had a rich metabolism that used different food sources, and it had internal organelles. So far, so familiar. But its genetics are a different story altogether.

For starters, LUCA may not have used DNA. Poole has studied the history of enzymes called ribonucleotide reductases, which create the building blocks of DNA, and found no evidence that LUCA had them (BMC Evolutionary Biology, DOI: 10.1186/1471-2148-10-383). Instead, it may have used RNA: many biologists think RNA came first because it can store information and control chemical reactions (New Scientist, 13 August, p 32).

The crucial point is that LUCA was a "progenote", with poor control over the proteins that it made, says Massimo Di Giulio of the Institute of Genetics and Biophysics in Naples, Italy. Progenotes can make proteins using genes as a template, but the process is so error-prone that the proteins can be quite unlike what the gene specified. Both Di Giulio and Caetano-Anollés have found evidence that systems that make protein synthesis accurate appear long after LUCA. "LUCA was a clumsy guy trying to solve the complexities of living on primitive Earth," says Caetano-Anollés.
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