A genome with a delete key
The deep ocean off the coast of California hosts an animal that challenges a basic principle of biology. The Pacific hagfish (Eptatretus stoutii) and its relatives are jawless eel-shaped creatures that belong to an ancient lineage of animals, the cyclostomes, that diverged from jawed vertebrates about 500 million years ago. For decades, scientists held that virtually every cell in a complex animal contains the exact same set of genetic instructions. Hagfish demonstrate a radical exception. During their embryonic development, the cells destined to become most of the hagfish's body—its somatic cells—systematically destroy and discard large portions of their own DNA. This process is called programmed genome rearrangement (PGR).
Only the germline cells, which become eggs or sperm, retain the complete, unabridged genome. The scale of this genetic deletion is significant. In the Japanese hagfish (Eptatretus burgeri), about 21% of the germline DNA is eliminated from somatic cells. Across different hagfish species, the amount of discarded DNA ranges from 20% to as high as 74.5%. The eliminated material consists of entire chromosomes or large chromosomal fragments, which contain many highly repetitive DNA sequences, often called satellite DNA. This process was first discovered through cytogenetic studies that noticed a stark difference in chromosome counts between germline and somatic tissues. For example, E. burgeri has 52 chromosomes in its reproductive cells but only 36 in its body cells.
An evolutionary strategy
The retained genome in the somatic cells contains all the necessary genes for day-to-day cellular functions. The deleted DNA includes repetitive sequences but also protein-coding genes. Research suggests that many of these eliminated genes have functions specific to the germline, such as germ cell development and maintenance. By removing these specialized genes from body cells, the hagfish may prevent genetic conflict between the needs of the soma and the germline.
This genomic streamlining may also be an energy-saving adaptation. Maintaining and replicating a larger genome requires more cellular resources. By shedding non-essential DNA from the trillions of somatic cells, the organism can operate more efficiently. While programmed DNA loss occurs in some invertebrates and single-celled organisms, its presence in a vertebrate like the hagfish is unique. The discovery forces a re-evaluation of how vertebrate genomes can evolve and function. Sequencing the full germline genome of the hagfish has been a challenge precisely because of its complexity and the masses of repetitive DNA that are later deleted. These studies provide information about the deep evolutionary history of all vertebrates, including humans.