In Hawaiian myth, the octopus is the lone survivor of an earlier, alien universe. If that were so, the octopus might be expected to have a neatly organized genome, one lacking any signs of having been reassembled from another world’s wreckage. But in fact the octopus has a genome that seems a more jumbled version of other, less bizarre organisms.
That’s just one observation that has come out of a genome sequencing project conducted by scientific teams from the University of Chicago, University of California, Berkeley, and Okinawa Institute of Science and Technology (OIST) as part of the Cephalopod Sequencing Consortium. This international collaboration was initiated by Nobel Laureate Sydney Brenner, founding president and a distinguished professor of OIST.
According to Brenner, one of the many reasons octopuses grab our attention is that “they were the first intelligent beings on the planet.” Octopuses, along with squids, cuttlefish and nautiluses, are cephalopods, a class of predatory molluscs with an evolutionary history spanning more than 500 million years (long before plants moved onto land). Inhabiting every ocean at almost every depth, they possess unique adaptations such as prehensile arms lined with chemosensory suckers, the ability to regenerate complex limbs, vertebrate-like eyes and a sophisticated camouflage system. With large, highly-developed brains, cephalopods are the most intelligent invertebrate and have demonstrated elaborate problem-solving and learning behaviors.
To study the genetics of these specialized traits, the international team of researchers sequenced the genome of the California two-spot octopus (Octopus bimaculoides) to a high level of coverage (on average, each base pair was sequenced 60 times). To annotate the genome, the team generated transcriptome sequence data—which can be used to measure gene expression based on RNA levels—in 12 different tissues types.
The results of this work appeared August 12 in Nature, in an article entitled, “The octopus genome and the evolution of cephalopod neural and morphological novelties.” Curiously, the octopus genome showed no indications of whole genome duplication events, which had been widely expected. Yet there were ample wonders of other sorts.
“The core developmental and neuronal gene repertoire of the octopus is broadly similar to that found across invertebrate bilaterians, except for massive expansions in two gene families previously thought to be uniquely enlarged in vertebrates: the protocadherins, which regulate neuronal development, and the C2H2 superfamily of zinc-finger transcription factors,” wrote the authors. “Extensive messenger RNA editing generates transcript and protein diversity in genes involved in neural excitability, as previously described, as well as in genes participating in a broad range of other cellular functions.
“We identified hundreds of cephalopod-specific genes, many of which showed elevated expression levels in such specialized structures as the skin, the suckers and the nervous system. Finally, we found evidence for large-scale genomic rearrangements that are closely associated with transposable element expansions.”
A unique feature of the octopus genome appears to be widespread genomic rearrangements. In most species, specific cohorts of genes tend to be close together on the chromosome. However, most octopus genes show no such connections. Hox genes, for example, control body plan development and cluster together in almost all animals. Octopus Hox genes are scattered throughout the genome with no apparent linkages.
The octopus genome is enriched in transposons, also known as “jumping genes,” which can rearrange themselves on the genome. While their role in octopuses is unclear, the team found elevated transposon expression in neural tissues. Transposons are known to affect the regulation of gene expression and play major roles in shaping genome structure.
“With a few notable exceptions, the octopus basically has a normal invertebrate genome that's just been completely rearranged, like it's been put into a blender and mixed,” said Caroline Albertin, co-lead author and graduate student in the Department of Organismal Biology and Anatomy at the University of Chicago. “This leads to genes being placed in new genomic environments with different regulatory elements, and was a completely unexpected finding.”