Lungfish genome discovery explains how fish first walked onto land

Let’s spend a few minutes time traveling back to the Devonian period, where we unravel the mysteries hidden within the lungfish genome — the world’s largest animal genome, and a treasure trove of information about one of evolution’s most pivotal transitions.

Picture yourself at the edge of a shallow sea, sometime between 420 and 360 million years ago. Here, an extraordinary event unfolded: a lobe-finned fish, propelled by its robust pectoral fins, hauled itself from the water onto dry land.

This remarkable creature, equipped with lungs capable of extracting oxygen from air, marked a turning point in Earth’s biological history.

It likely represents the first venture of a vertebrate onto land – a momentous step that paved the way for the diverse array of terrestrial vertebrates we see today, including amphibians, reptiles, birds, and mammals like ourselves.

But what gave these lobe-finned fishes their unique ability to conquer the challenges of a terrestrial environment? The answer lies hidden within their genetic code, waiting to be deciphered.

Genetic legacy of our ancestral cousins

In an endeavor to solve this longstanding mystery, scientists have analyzed the genetic material of the closest existing relatives of our Devonian ancestor.

These relatives are the lungfish, only three lineages of which survive today: one in Africa, one in South America, and one in Australia.

These ancient “living fossils” bear an uncanny resemblance to their ancestors, providing a glimpse into evolutionary history.

To decode the lungfish genomes, knowledge of their complete sequences is critical, as DNA is made up of nucleobases and the order of these nucleobases carries the essential genetic information.

Even though it was known that lungfish genomes were enormous, the precise scale and what could be inferred from them weren’t clear until now.

Deciphering lungfish genome

Decoding the genomes of lungfish posed significant challenges, both technically and bioinformatically.

However, an international team of researchers, led by biologist Dr. Axel Meyer from the University of Konstanz and biochemist Dr. Manfred Schartl from Würzburg, managed to completely sequence the genome of the South American lungfish and a member of the African lineage.

Dr. Meyer highlighted the nature of their findings. He noted that the South American lungfish species possesses an extraordinary genome.

“With over 90 gigabases (in other words, 90 billion bases), the DNA of the South American species is the largest of all animal genomes,” he explained. This genetic blueprint is more than double the size of the previous record holder, the Australian lungfish.

Dr. Meyer went on to emphasize the sheer scale of this discovery, pointing out that “18 of the 19 chromosomes of the South American lungfish are each individually larger than the entire human genome.”

To put this into perspective, he reminded us that the human genome contains nearly 3 billion bases, underscoring the immense complexity of the lungfish’s genetic material.

Unanticipated lungfish genome expansion

The expansive size of the lungfish genome is attributed to autonomous transposons, DNA sequences that reproduce and change their location within the genome, leading to genome expansion.

Although common in other organisms, the researchers found that the expansion rate of the South American lungfish genome is the fastest on record.

Dr. Meyer stated, “Every 10 million years in the past, its genome has grown by the size of the entire human genome. And it continues to grow. We have found evidence that the transposons responsible are still active.”

The team uncovered the underlying cause for the extraordinary expansion of this genome. Their research revealed that the massive growth is primarily attributed to a significantly reduced presence of piRNA.

This particular type of RNA typically plays a crucial role in a molecular process that suppresses transposons.

However, with the scarcity of piRNA in this species, the usual silencing mechanism appears to be compromised, potentially allowing for unchecked genome expansion.

Stability amidst an explosion of transposons

Despite the vast surplus of transposons and the contribution they make to genome growth, the researchers observed no correlation between the enormous transposon surplus and genome instability.

In fact, the lungfish genome was surprisingly stable, and the gene arrangement remarkably conservative, allowing the researchers to reconstruct the ancestral tetrapod’s original chromosome framework from the lungfish species that are still alive today.

This new research also enabled the scientists to understand the genetic basis of the differences between the existing lineages.

For instance, the Australian lungfish still possesses the limb-like fins which once allowed its relatives to tread on land.

These fins, similar in structure to our arms, evolved back into filamentous fins over the last 100 million years or so in the other existing lungfish species from Africa and South America.

Diving deeper

To further investigate this evolution, the team conducted additional experiments. “In our research, we also used experiments with CRISPR-Cas transgenic mice to show that this simplification of the fins is attributable to a change in what is known as the Shh-signaling pathway,” Dr. Meyer explained. This pathway plays a crucial role in embryonic development.

“During the embryonic development of mice, for example, the Shh-signalling pathway controls the number and development of the fingers, among other things,” added Dr. Meyer.

These findings provide additional evidence of the evolutionary link between the ray fins of bony fish and the fingers of land vertebrates.

With the entire genome sequences of all current lungfish families now available, future comparative genomic studies will provide deeper insights into the lobe-finned ancestors of land vertebrates – potentially cracking the code of how vertebrates transitioned onto land.

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