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Tunicate Genome Sequence Reveals Genomic Diversity in Chordates

By Andrea Anderson

NEW YORK (GenomeWeb News) – In a paper appearing online today in Science, an international team reported that it has sequenced the genome of the larvacean tunicate Oikopleura dioica, uncovering a range of genome features — from gene order to intron patterns — not previously reported in other animals.

"[M]ultiple genome organization features, conserved across metazoans including other tunicate and non-bilaterians, have dramatically changed in the Oikopleura lineage," co-corresponding author Daniel Chourrout, research director of the University of Bergen's Sars International Centre for Marine Molecular Biology, and co-authors wrote.

Together, the findings underscore the rapid evolution and dramatic genome changes that have occurred in the lineage leading to O. dioica, an organism that is more simplified in some respects than less derived animals in the same lineage, Chourrout told GenomeWeb Daily News.

Such changes may have stemmed, in part, from the organism's lifestyle — particularly exposure to UV radiation — coupled with an apparent dearth of DNA repair mechanisms, he noted.

Tunicates, in general, are chordate animals found in a sister lineage to vertebrates. But in contrast to Ciona, the first tunicate to have its genome sequenced, O. dioica belongs to a group of larvacean tunicates found in marine zooplankton that retain larvae-like features even as adults.

O. dioica filter feed in groups using a secreted "house" structure that eventually becomes clogged with food and waste material and sinks to the bottom of the ocean, Chourrout explained, contributing to carbon flux in the ocean.

The researchers used shotgun sequencing to sequence the compact, 70 million base O. dioica genome to 14 times coverage using DNA isolated from male tunicates generated through 11 sibling pair matings intended to create an inbred tunicate line.

Despite its diminutive size, the team estimates that the tunicate genome houses 18,020 protein-coding genes that are packed into the genome thanks to an abundance of operons, miniscule intergenic regions, and a preponderance of genes with small introns.

Certain groups of genes do have larger introns and intergenic spaces, the team noted, including genes coding for developmentally regulated transcription factors and several Y chromosome genes expressed during the process of sperm development in tunicate testis.

But overall, Chourrout explained, the tunicate genome showed architectural and organizational patterns distinct from those seen in animals whose genomes have been characterized so far.

For instance, he said, the O. dioica genome has apparently undergone extreme changes in gene order, losing much of the synteny seen in other animals. The tunicate shares even less gene order conservation with humans than do sponges, Chourrout said, explaining that Oikopleura would form a phylogenetic tree external to all other animals based on its gene order alone.

"There were probably a lot of [DNA] breaks during the evolution of this genome. And we have observed that there may also be a deficiency in the DNA repair," he said. "So that could be a reason why the order of genes is changed."

Although the number of introns per gene is comparable to that found in other animals, the team found, the introns that are present in the tunicate genome are largely distinct from those believed to have been present in the common ancestor of tunicates and vertebrates.

Roughly six out of every seven old or ancestral introns have been lost in O. dioica, Chourrout explained, and many have been replaced by new, more recently evolved introns.

"We were extremely surprised to see this complete change in intronic zone organizations," Chourrout said. "Because this is also placing this animal completely outside of what we see in all other animals."

Moreover, the intron patterns themselves are offering new clues about the mechanism of intron gain, Chourrout explained. For example, the researchers identified introns that share sequence homology with one another, hinting that introns are capable of propagating within genes.

Compared to other animals, the O. dioica genome also contains very few transposable elements, the team found — a finding consistent with tunicate's petite genome size.

"Typically a compact genome would be refractory to transposons," Chourrout said. "The genome is eliminating the old transposons and what you see is just the fresh ones, the new invaders."

Unexpectedly, though, the researchers found examples of gene families that have expanded in O. dioica, including extensive duplications of some developmental genes.

Although more research is needed to understand these duplications — and the consequences of other genome changes detected in O. dioica — those involved in the study say their findings highlight the genomic diversity that can exist in organisms with similar morphological features.

"Despite an unprecedented genome revolution, the Oikopleura lineage preserved essential morphological features, even maintaining the chordate body plan to the adult stage, unlike other tunicates," the authors noted. "Our results strengthen the view that global similarities of genome architecture from sponge to human are not essential for the preservation of ancestral morphologies, as is widely believed."

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