One of the stranger forms of life on our planet is the tiny, torpedo-shaped chaetognath, which roams the seas on the hunt for small crustaceans. These predators are named after the chitinous grasping spines surrounding their mouth (Greek: "chaite", bristle, and "gnathos", jaw), and are also known as arrow worms.
Despite their ubiquity in the world's oceans, the evolutionary origin of this unique lifeform has long baffled biologists – Charles Darwin himself noted their "obscurity of affinities" in 1844. Notably, the worm has characteristics of both protostomes, which include arthropods, mollusks, and annelids, and deuterostomes, which covers all animals with a spinal cord. These two groups are thought to have diverged from a common ancestor in the Ediacaran era, about 600 million years ago.
But now, researchers from University College London (UCL), the Goto Laboratory at Mie University, and the Okinawa Institute of Science and Technology (OIST) have finally pinned down the genomic, epigenomic, and cellular landscape of this enigmatic animal in a study published in Nature. As a planktonic animal, they are almost impossible to culture in the lab – save for one species, Paraspadella gotoi, named in honor of Professor Taichiri Goto, who is the first to successfully breed chaetognaths.
Shuffling genes
By zooming in on P. gotoi, the researchers found that despite retaining a similar body shape since the Cambrian period hundreds of millions of years ago, the chaetognath genome has evolved at breakneck speed, leading to a highly unique genetic markup. And thanks to single-cell RNA sequencing, the researchers were able to connect the unique genetic markup directly to specialized cell-types found throughout the chaetognath body, tied to their unique morphology and predatory lifestyle.
"While most animals tend to use the same set of genes inherited from the last common ancestor, chaetognaths underwent an extreme reshuffling of their gene complement, essentially inventing a lot of new genes, such as ones for unique sensory cell types involved in the perception of movement in the water column," explains Dr. Ferdinand Marlétaz, senior author and researcher at UCL, whose work started at OIST. "More generally, our study also shows how some animal groups can diverge by their molecular pathways."
The team discovered that in addition to an unprecedented rate of both de novo gene genesis and gene duplication, both of which are hallmark catalysts of evolutionary diversification, the chaetognath lacks genes for the assembly of the centromeres – the regions often at the center of chromosomes that are vital for accurate genome transmission during cell divisions. And yet, they were found to still possess centromeres, suggesting a unique method of chromosomal organization. These are just some of the unusual characteristics of the genome and molecular markup characterized by the team, who also verified the once-controversial classification of chaetognaths as early spiralians, sharing the group with mollusks, annelids and flatworms.
"With this data, we have been able to accurately describe the evolutionary developmental genomics of arrow worms and correlate it directly with cell types," says Professor Noriyuki Satoh of the Marine Genomics Unit at OIST . "These methods have previously been reserved for well-studied model animals like nematodes and fruit flies. With this paper, we have solidified the possibility of applying these methods to the entire animal kingdom, bringing us closer to truly understand the evolution of life."
