COLD SPRING HARBOR, NEW YORK—Going from one cell to many all in one organism was no easy feat. Multicellularity required molecular machinery that made it possible for cells to stick and work together. They needed to be able to talk to one another and to recognize and deter intruder cells.
But the last unicellular ancestor of animals was ready to make that leap. And even the most ancient multicellular animals were equipped with a skeleton crew of the genes that made the diversity of animal forms seen today possible. That was the news from the Cold Spring Harbor Symposium “Evolution: The Molecular Landscape,” held from 27 May to 1 June. Two teams have reached down to the base of the animal tree of life to learn how this key evolutionary transition occurred.
Nicole King of the University of California, Berkeley, and her colleagues use choanoflagellates as stand-ins for the last unicellular ancestor of animals. These single-celled creatures look and function a lot like cells called choanocytes in sponges. A flagellum sticks out of one end, whipping up water currents to circulate bacteria back toward a "collar" that slurps up the microbes. Some of the 150 species form colonies (left), approximating multicellular life.
A choanoflagellate genome, published last year, revealed genes for proteins that animals use for cell adhesion and signaling, and King has been looking into what those genes do in single-celled organisms. From those studies, she says, "we can learn some basic mechanisms of what was in place in the common ancestor."
One surprise in the genome were two dozen genes for cadherins, proteins that are critical for holding cells together in all animals. If cadherin genes are disabled during development, the embryo falls apart. Such genes had never been found outside a multicellular animal before. "We think [cadherins] are distinguishing different prey," King reported at the meeting. She and her colleagues have been examining these cadherin genes one by one. They have determined that some cadherin genes are active in the collar. They also find the amount of a particular cadherin protein depends on what bacteria are present in the surrounding water. For example, three cadherins are upregulated in the presence of flavobacter microbes but not when enterobacter bacteria are present, whereas the concentrations of other cadherins are unaffected.
King suspects that cadherin senses and binds to the bacteria, as some pathogenic microbes dock at cadherins to invade human cells. "[Choanoflagellates] have systems in place that allowed cell-cell recognition. [We] can see how one could evolve into a multicellular organism by using [these proteins] in a different way," says Bruce Stillman, president of Cold Spring Harbor Laboratory in New York.
Choanoflagellates were a prelude to sponges, which evolved 600 million years ago and as such are the oldest extant animals. Sponges split off from the animal tree of life early on and maintained their simple body plan—sans muscles and a nervous system—while the eumetazoans evolved wings, fins, feet, heads, and tails to create the myriad of shapes and sizes seen in the animal kingdom today. By looking at the newly sequenced genome of one sponge, Amphimedon queenslandica (left), and choanoflagellates, "we can appreciate how multicellular organisms came about," says Stillman.
The protoanimal genome was quite busy during the more than 100 million years between choanoflagellates and the evolution of sponges. Bernard Degnan of the University of Queensland, Brisbane, Australia, and his colleagues have looked for what's common to all the animal genomes, concluding that they share about 5000 ancestral gene families, 1300 of which must have evolved during that time because they have no representatives in the choanoflagellates yet are found in sponges. For example, most of the genes needed to make the epithelium, which separates an organism from the outside world, appeared first in the sponge. In other gene families, in which choanoflagellates have a single gene, the families have expanded in sponges and sometimes exploded in more complex animals.
The sponges have precursors to some of the key development genes. One called hedgling codes for a protein that's like the signaling molecule called hedgehog, but it's locked to the cell membrane and cannot travel from cell to cell as does hedgehog. Hedgling "is still probably a signaling molecule but plays a different role," Degnan reported.
What sponges seem to lack is complex regulation of all these genes. In other animals, genes are often used in multiple contexts, but this is not the case for the sponge, says Degnan. Its genome is compact, with little room for regulatory DNA in between genes. This regulatory simplicity, he adds, "may be the key to why the [sponge] body plan has not changed" for 600 million years.
Credits: Choanoflagellate Colony, Mark Dayel; Sea Sponge, Gemma Richards