From a single-celled creature, a vast kingdom arose

Published 5:00 am Monday, March 21, 2011

Lurking in the blood of tropical snails is a single-celled creature called Capsaspora owczarzaki. This tentacled, amoebalike species is so obscure that no one even noticed it until 2002. And yet, in just a few years, it has moved from anonymity to the scientific spotlight. It turns out to be one of the closest relatives to animals. As improbable as it might seem, our ancestors a billion years ago probably were a lot like Capsaspora.

The origin of animals was one of the most astonishing and important transformations in the history of life. From single-celled ancestors, they evolved into a riot of complexity and diversity. An estimated 7 million species of animals live on earth today, ranging from tubeworms at the bottom of the ocean to elephants lumbering across the African savanna. Their bodies can total trillions of cells, which can develop into muscles, bones and hundreds of other kinds of tissues and cell types.

The dawn of the animal kingdom about 800 million years ago was also an ecological revolution.

Animals devoured the microbial mats that had dominated the oceans for more than 2 billion years and created their own habitats, like coral reefs.

The origin of animals is also one of the more mysterious episodes in the history of life. Changing from a single-celled organism to a trillion-cell collective demands a huge genetic overhaul. The intermediate species that might show how that transition took place have become extinct.

“We’re just missing the intervening steps,” said Nicole King, an evolutionary biologist at the University of California, Berkeley.

To understand how animals took on this peculiar way of life, scientists are gathering many lines of evidence. Some use rock hammers to push back the fossil record of animals by tens of millions of years. Others are finding chemical signatures of animals in ancient rocks. Still others are peering into the genomes of animals and their relatives like Capsaspora, to reconstruct the evolutionary tree of animals and their closest relatives. Surprisingly, they’ve found that a lot of the genetic equipment for building an animal was in place long before the animal kingdom even existed.

It was only in the past few years that scientists got a firm notion of what the closest relatives to animals actually are. In 2007, the National Human Genome Research Institute started an international project to compare DNA from different species and draw a family tree. The cousins of animals turn out to be a motley crew. Along with the snail-dwelling Capsaspora, our close relatives include choanoflagellates, amoebalike creatures that dwell in fresh water, where they hunt for bacteria.

How did it happen?

Now scientists are trying to figure out how a single-celled organism like Capsaspora or choanoflagellates became a multicellular animal. Fortunately, they can get some hints from other cases in which microbes made the same transition. Plants and fungi evolved from single-celled ancestors, as well as dozens of other less familiar lineages, from brown algae seaweed to slime molds.

Primitive multicellularity may have been fairly easy to evolve. “All that has to happen is that the products of cell division stick together,” said Richard Michod of the University of Arizona. Once single-celled organisms shifted permanently to colonies, they could start specializing on different tasks. This division of labor made the colonies more efficient. They could grow faster than less specialized colonies.

Eventually, this division of labor could have led many cells in proto-animals to give up their ability to reproduce. Only a small group of cells still made the proteins required to produce offspring. The cells in the rest of the body could then focus on tasks like gathering food and fighting off disease.

“It’s not a hurdle,” said Bernd Schierwater of the University of Veterinary Medicine in Hanover, Germany. “It’s a very good way to be very efficient.”

To figure out how animals evolved, researchers are now sequencing the genomes of their single-celled relatives. They’re discovering a wealth of genes that were once thought to exist only in animals. Inaki Ruiz-Trillo of the University of Barcelona in Spain and his colleagues searched Capsaspora’s genome for an important group of genes that encode proteins called transcription factors. Transcription factors switch other genes on and off, and some of them are vital for turning a fertilized egg into a complex animal body.

In the current issue of Molecular Biology and Evolution, Ruiz-Trillo and his colleagues report that Capsaspora shares a number of transcription factors that were once thought to be unique to animals. For example, they found a gene in Capsaspora that’s nearly identical to the animal gene brachyury. In humans and many other animal species, brachyury is essential for embryos to develop, marking a layer of cells that will become the skeleton and muscles.

Ruiz-Trillo and his colleagues have no idea what Capsaspora is doing with a brachyury gene. They’re now doing experiments to find out; in the meantime, Ruiz-Trillo speculates that single-celled relatives of animals use the brachyury gene, along with other transcription factors, to switch genes on for other tasks.

“They have to check out their environment,” said Ruiz-Trillo. “They have to mate with other organisms. They have to eat prey.”

Studies by other scientists point to the same conclusion: a lot of the genes once thought to be unique to the animal kingdom were present in the single-celled ancestors of animals. “The origin of animals depended on genes that were already in place,” King said.

In the transition to full-blown animals, King argues, these genes were co-opted for controlling a multicellular body. Old genes began to take on new functions, like producing the glue for sticking cells together and guarding against runaway cells that could become tumors.

Shuffling proteins

Despite their seeming simplicity, sponges are card-carrying members of the animal kingdom. Like other animals, sponges can produce eggs and sperm, which can then produce embryos. Sponge larvae swim through the water to find their way to a good spot where they can settle down for a sedentary life and grow into adults. Their development is an exquisitely sophisticated process, with stem cells giving rise to several different cell types.

The first sponge genome was only published in August. It offered scientists an opportunity to compare the DNA of sponges to that of other animals as well as to Capsaspora and other single-celled relatives. The researchers looked at each gene in the sponge genome and tried to match it to related groups of genes in other species, known as gene families. All told, they were able to find 1,268 gene families shared by all animals — including sponges — but not by other species.

Those genes were presumably passed down to living animals from a common ancestor that lived 800 million years ago. And by surveying this catalog, scientists can infer some things about what that ancestor was like.

“It wasn’t just an amorphous blob of cells,” said Bernard Degnan of the University of Queensland. Instead, it was already setting aside eggs and sperm. It could produce embryos, and it could lay down complicated patterns in its body.

Animals didn’t just evolve multicellular bodies, however. They also appear to have evolved new ways of generating different kinds of bodies. Animals are more prone to mutations that shuffle sections of their proteins into new arrangements, a process called domain shuffling. “Domain shuffling seems to be a critical thing,” Degnan said.

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