How the coelacanth has recently developed dozens of new genes

The capture of the first living Coelacanth, a powerful ocean predator, off the coast of South Africa caused a great stir in 1938, 65 million years after its supposed extinction. It was known as a ‘living fossil’ because of its anatomy which looks almost identical to the fossil record. But although the body of the coelacanth has changed little, its genome tells a different story.

Scientists from Toronto have now revealed that the African coelacanth, Latimeria chalumnae, acquired 62 new genes through encounters with other species 10 million years ago. Their findings are reported in the journal Molecular biology and evolution.

What is even more fascinating is how these genes originated. Their series suggest that they originated from transposons, also known as ‘selfish genes’. These are parasitic DNA elements whose sole purpose is to make more copies of themselves, which they sometimes achieve by moving between species.

The findings show the dramatic effect that transposon DNA can have on gene creation and provide a glimpse into some of the forces that shaped the genome of one of the oldest and most mysterious organisms.

“Our findings provide a rather striking example of this phenomenon of transposition that contributes to the genome of the host,” said Tim Hughes, senior study author and a professor of molecular genetics at the Donnelly Center for Cellular and Biomolecular Research at the University of Toronto.

“We do not know what these 62 genes do, but many of them encode DNA-binding proteins and probably play a role in gene regulation, where even subtle changes are important in evolution,” says Hughes, who is Canada’s research chair in decoding. Gene Regulation and John W. Billes Chair of Medical Research at the Temerty Faculty of Medicine at U of T.

Transposons are also sometimes called “jumping genes” because they change location in the genome, thanks to a self-encoded enzyme that recognizes and moves its own DNA code via a ‘cut and paste’ mechanism. New copies can arise through serendipitous jumps during cell division when the entire genome is repeated.

Over time, the enzyme’s code expires and the jump stops. But if the changed sequence offers even a subtle selective advantage to the host, it can start a new life as a bona fide host gene.

There are plenty of examples of transposon-derived genes across different species, but the Coelacanth is striking by its scale.

“It was surprising to see that coelacanths among vertebrates have a large number of these transposon-derived genes because they have an undeserved reputation for being a living fossil,” said graduate student Isaac Yellan, who headed Has of the study.

“The coelacanth may have developed a little slower, but it’s definitely not a fossil,” he says.

Yellan made the discovery while looking for peers in other species of a human gene he studied. He knew that the gene, CGGBP1, originated from a specific type of transposon in the common ancestor of mammals, birds and reptiles. It is named after the protein it encodes, which binds CGG-containing DNA sequences, but it was difficult to study in part because it has no counterpart in other species that are frequently studied, such as fruit flies.

After scanning all available genomes, Yellan was able to find related genes, but its distribution across the species was unstable and not what you would expect from normal ancestry. In addition to the single CGGBP-like gene in all mammals, birds, and reptiles, Yellan found specimens in some, but not all, fish he looked at, as well as in lamprey, a primitive vertebrate, and some kind of fungus. Worms, mollusks and most insects had nothing. And then there were 62 in the Coelacanth, the genome of which became available in 2013.

Since the general origin is excluded, it appears that the transposers came in different descendants at different times by carrying between species through the horizontal gene transfer.

“Horizontal gene transfer blurs the picture of where the transpons come from, but we know of other species that can occur via parasitism,” says Yellan. “The most likely explanation is that they have been introduced several times throughout evolutionary history.”

It remains unclear what the genes do, but several pieces of evidence point to a finely tuned role in gene regulation. Computational modeling and test tube experiments determined that the gene’s products are proteins that bind unique sequence signatures on the DNA, suggesting a role in gene expression, similar to the human counterpart. Furthermore, the genes are switched on alternately across a dozen data cell organs for which data exist, indicating fine-tuned roles that are tissue-specific.

Where the genes originally came from and what they do in the Coelacanth can remain a mystery. Research specimens are only occasionally pulled up by fishing boats and it took until 1998 to discover the other known living species, Latimeria menadoensis, in an Indonesian fish market.

The species split before the new genes appeared, excluding them to cause specification. Yet they may have formed the African coelacanth we know today, with its majestic armor of royal blue scales casting shadows on its tan family member, Yellan said, which is pure speculation.

Alas, we may never find out.

“The coelacanths are extremely rare,” says Yellan. “And they can hide very well.”

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