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Coelacanth Genome Confirms Sluggish Gene Changes in Lobe-finned Fish

NEW YORK (GenomeWeb News) – The fleshy-finned African coelacanth may carry many of the same gene coding sequences that its ancient ancestors did, according to a genome sequencing study out today in Nature.

A large international team led by investigators in the US, Germany, and Sweden put together a draft genome assembly for the African coelacanth, Latimeria chalumnae. To aid in their analyses, the group also folded in transcriptome sequence data on tissues from both African and Indonesian coelacanths.

The team's phylogenetic tree — produced using a subset of the protein coding sequences — indicated that coelacanth genes tend to have low substitution rates relative to those in other animals.

It also pointed to more distant genetic ties between the coelacanth and four-legged land animals than there are between the lungfish, another, yet-to-be sequenced fleshy-finned fish, and tetrapods. Nevertheless, the newly sequenced genome provided a glimpse at some of the sensory, excretory, and immune system patterns that may have existed in animals before their adaptation to land, study authors said.

"Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion," they wrote, "and the development of fins, tail, ear, eye, brain, and olfaction."

Coelacanths have inspired a great deal of curiosity amongst biologists since their discovery in the late 1930s. The large fish have limb-like or "lobed" fins, along with other physical features that — at least outwardly — resemble those found in skeletons of ancient fish believed to have lived at least 300 million years ago.

These and other patterns have prompted speculation that modern-day coelacanths, found mainly off of Africa's East Coast, are the product of somewhat plodding evolutionary processes, perhaps reflecting successful early environmental adaptation within the coelacanth lineage.

"We often talk about how species have changed over time," co-senior author Kerstin Lindblad-Toh, director of the Broad's vertebrate genome biology group, said in a statement. "But there are still a few places on Earth where organisms don't have to change, and this is one of them."

"Coelacanths are likely very specialized to such a specific, non-changing, extreme environment," she added. "It is ideally suited to the deep sea just the way it is."

She and her colleagues used Illumina instruments to sequence genomic DNA from a coelacanth specimen collected near the Comoros Islands, east of Mozambique. The sample had been obtained roughly a decade ago. But given the scarcity of the sample and the difficulty involved in obtaining material from the endangered fish, researchers held off on sequencing it until the advent of high-throughput sequencing technologies that required little starting material.

To augment this genome sequence information, they also performed RNA sequencing on fresh tissue samples from an Indonesian coelacanth and on other decades-old samples from an African coelacanth — data that proved useful for genome annotation and subsequent analyses.

All told, the team found more than 29,000 predicted protein-coding genes in the 2.86 billion base draft coelacanth genome assembly, along with nearly 2,900 short non-coding RNAs, some 1,200 long non-coding RNAs, and tens of thousands of conserved RNA secondary structures.

Despite the apparent physical similarities between the coelacanth's fleshy fins and tetrapod limbs, though, the research group's phylogenetic analyses suggest that it was ancestors of the lungfish that most likely made the first forays onto land.

In particular, when they compared a set of coelacanth transcripts to orthologous RNA sequences from 21 other jawed vertebrate species that included a West African lungfish, the investigators saw signs that the lungfish lineage is more closely related to existing four-limbed creatures than the coelacanth lineage is.

Sequence comparisons across the animal phylogeny also highlighted the particularly low substitution rate of coding sequences within the coelacanth genome, though there were hints that non-coding regions of the genome may have evolved more quickly.

"We showed that there was slow evolution of the protein-coding genes, but in every other measure we looked at, it did not look particularly slow," the Broad Institute's Jessica Alföldi, co-first author on the study, told GenomeWeb Daily News.

At the moment it's difficult to look at the non-coding sequences in detail, she noted, given difficulties in precisely aligning those with sequences from other animals. Even so, Alföldi added, the coelacanth genome appears to be home to a good deal of transposable element activity, not to mention large-scale sequence rearrangements.

The apparent difference in evolutionary change between coding and non-coding regions of the genome may reflect a relative lack of selective pressure in the coelacanth's current deep-sea cave environment, Alföldi said, though that still needs to be determined experimentally.

"[The coelacanth] lives in an environment where there's probably very few predators and not much in the way of competition for food," she said. "So it may not face the same kind of adaptive pressure that most other organisms have to deal with on a day-to-day basis."

By using coelacanth as a rough stand-in for ancestral creature that preceded tetrapods, meanwhile, researchers were able to find functional groups of genes that have appear to have changed in four-legged animals since their split from the coelacanth lineage.

Along with genes involved in limb development, for instance, the team saw shifts in regulatory elements near genes contributing to animals' sense of smell that would theoretically be compatible with a move from sea to land, Alföldi said.

Other genetic changes that are apparently associated with the transition to land turned up in pathways related to immune system function and the urea cycle — again consistent with the distinct environmental situation that animals face on land, where different pathogens exist and nitrogen waste isn't secreted directly into a surrounding sea environment.