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7-Jul-2008 17:00 Eastern US Time

Single but chatty

LA JOLLA, CA — In a many-celled organism, cells signal to each other all the time, because several trillion cells all doing their own thing wouldn't be an animal, a plant or a human. It would be a disaster.

So it is clear why the cells in our body need lots of machinery for sending signals to each other. What isn't obvious is why an organism that is just one cell would need more signalling machinery than humans have.

Single cells in the sea

Yet this is what scientists at the Salk Institute for Biological Studies have found in a beast called Monosiga brevicollis. This single-celled organism lives in the sea and is eaten by krill, the main food of whales. It belongs to the group known as choanoflagellates, which are microscopic, aquatic creatures that occupy the grey area between fungi and animals. They live on bacteria.

Choanoflagellates are scientifically important because they shared a common ancestor with animals, between 600 million and a billion years ago. So they can help us understand the origins and evolution of animals.

Earlier this year biologist Nicole King at the University of California, Berkeley and a number of colleagues published papers on Monosiga brevicollis. They had just sequenced its genome.

Surprise, surprise

One finding that surprised them was that Monosiga has many genes that in animals make cells stick together. Since Monosiga is just one cell and does not form colonies the scientists were at a loss to explain this.

A couple of months earlier King and Sean Carroll from the University of Wisconsin, Madison had published another Monosiga surprise. They had found that the little protist has a type of protein known as a tyrosine kinase in its single cell. This was the first time these had been discovered outside metazoans.

The 100 trillion cells in our bodies need clever communication systems to work together. Tyrosine kinases are a vital part of this system. They are molecular sensors that nestle in the cell membrane. When a chemical from ouside plugs into the receptor, like a key into a lock, a signal pathway becomes active inside the cell.

In this way kinases allow cells to receive signals that tell them when to grow, when to stay the same and even when to die.

So surprise number two was that Monosiga has a tyrosine kinase, which is used for sending signals between cells. But it only has one cell.

Surprise

Now comes surprise number three from Gerard Manning and his colleagues at the Salk Institute's Razavi-Newman Center for Bioinformatics. Monosiga can make more than one type of tyrosine kinase, they have discovered. In fact the little cell has 128 different tyrosine kinase genes. This is 38 more than we humans have.

The study will be published during the week of July 7-11 in the onlinef edition of the Proceedings of the National Academy of Science

This treasure-trove of diverse and novel tyrosine kinases took the scientists by surprise, says the study's lead author Gerard Manning. "We were absolutely stunned. Based on past work we had expected maybe a handful of these kinases.

"But instead we discovered that this primitive organism has a record number of them. Two other essential parts of the tyrosine kinase network - PTP and SH2 genes - are also more numerous than in any other genome, showing that it is the whole network that is elaborated here."

Kinase and cousins

Monosiga brevicollis seems to have little in common with many-celled animals that need to coordinate the activities of billions or trillions of cells. But although just one cell Monosiga has quite a complex architecture. A collar of tentacle surrounds a whip-like tail known as a flagellum.

This is the same basic structure as in collar cells that clump together to form sponges, the most primitive many-celled organisms.

Its key evolutionary position is the reason Monosiga brevicollis has been selected by scientists as a good choanoflagellate for whole-genome sequencing. "Choanoflagellates are like first cousins of animals and their genome allows us a glimpse into the evolutionary origin of animals," says Manning.

The Monosiga kinases may help scientists understand how all tyrosine kinase signalling works. Despite their diversity, Monosiga kinases time and again arrive at the same solution to a problem as do animal kinases.

But they use distinct methods, for instance to create a sensor structure or to target a kinase to a specific part of a cell. "This convergent evolution suggests that there are only a limited number of ways build a functional network from these components," says Manning.

Why?

With all this new information, one obvious question remains unanswered. What is a single-celled organism doing with all this communications gear?

"We don't have a clue!" says Manning. "But this discovery is the first step in finding out."

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