Summary: Neural tissues of octopuses have a massively expanded miRNA repertoire, reflecting a similar evolution to that occurring in vertebrates. The findings suggest that miRNA play an important role in the development of complex brains.
Cephalopods, such as octopuses, squids, and cuttlefish, are highly intelligent animals with complex nervous systems. A team in Advances in Science led by Nikolaus Rajewski of the Max Delbrück Center has now shown that their evolution is linked to a dramatic expansion of the microRNA repertoire.
If we go back far enough in evolutionary history, we encounter the last known common ancestor of humans and cephalopods: a primitive worm-like animal with minimal intelligence and simple eyespots.
The animal kingdom can then be divided into two groups – vertebrates and non-vertebrates.
While vertebrates, especially primates and other mammals, have evolved large and complex brains with various cognitive abilities, invertebrates have not.
With one exception: cephalopods.
Scientists have long wondered why such a complex nervous system was able to develop only in these mollusks. Now, an international team led by researchers from the Max Delbrück Center and Dartmouth College in the US has revealed a possible reason.
in the article published inAdvances in science”, they explain, octopuses have a massively expanded microRNA (miRNA) repertoire in their neural tissues, mirroring similar developments in vertebrates. “So that’s what connects us to the octopus!” says Professor Nikolaus Rajewski, Scientific Director of the Institute for Medical Systems Biology of the Max Delbrück Center (MDC-BIMSB) Berlin, head of the Systems Biology Laboratory of Gene Regulatory Elements and last author of the paper. He explains that this finding likely means that miRNAs play a key role in the development of complex brains.
In 2019, Rajewski read a publication about genetic analyzes of octopuses. Scientists have discovered that a lot of RNA editing takes place in these cephalopods – meaning they make extensive use of certain enzymes that can recode RNA.
“This made me think that octopuses are not only good at editing, but may also have other RNA tricks,” Rajewsky recalls. So he began a collaboration with the marine research station Stazione Zoologica Anton Dohrn in Naples, sending him 18 different tissue samples from dead octopuses.
The results of this analysis were surprising: “There was indeed a lot of RNA editing going on, but not in the areas we were interested in,” says Rajewsky.
The most exciting discovery was actually the dramatic expansion of the famous group of RNA genes, the microRNAs. A total of 42 new miRNA families were found – especially in neural tissue and mainly in the brain.
Given that these genes have been conserved throughout the evolution of cephalopods, the team concludes that they are clearly beneficial to animals and therefore functionally important.
Rajewski has been researching miRNAs for over 20 years. Instead of being translated into messenger RNAs that deliver instructions for protein production in the cell, these genes encode small pieces of RNA that bind to the messenger RNA and thus affect protein production.
These binding sites have also been conserved during cephalopod evolution—another indication that the novel miRNAs are functionally important.
Novel microRNA families
“This is the third largest expansion of microRNA families in the animal kingdom and the largest outside of vertebrates,” says lead author Grigory Zolotarov, a Ukrainian scientist who interned in Rajewski’s lab at MDC-BIMSB while completing medical school in Prague. , and then.
“To give you an idea of the scale, oysters, which are molluscs, have acquired only five new microRNA families since their last shared ancestor with octopuses—while octopuses have acquired 90!” Zolotarov adds that oysters are not known for their intelligence.
Rajewski’s fascination with octopuses began years ago during an evening visit to the Monterey Bay Aquarium in California. “I saw this creature sitting at the bottom of the tank and we spent a few minutes – so I thought – looking at each other.”
He says that looking at an octopus is very different from looking at a fish: “It’s not very scientific, but there’s a sense of intelligence coming out of their eyes.” Octopuses have similarly sophisticated “camera” eyes to humans.
From an evolutionary perspective, octopuses are unique among invertebrates. They have both a central brain and a peripheral nervous system that can function independently. If an octopus loses a tentacle, the tentacle remains sensitive to touch and can still move.
The reason octopuses evolved such complex brain functions on their own may be because they have multi-purpose uses for their arms – for example, as tools for opening shells.
Octopuses also show other signs of intelligence: They are very curious and can remember things. They also get to know people and actually like some more than others.
Researchers believe that they are dreaming because they change their color and skin texture when they are already asleep.
“They say if you want to meet an alien, go scuba diving and make friends with an octopus,” Rajewsky said.
He now plans to join forces with other octopus researchers, creating a European network that will allow greater exchange between scientists. Although the community is currently small, Rajewsky says interest in octopuses is growing around the world, including among behavioral researchers.
He says that it is very interesting to analyze an advanced form of intelligence completely independent of our own. But it’s not easy: “If you experiment with them using small snacks as rewards, they soon lose interest. At least, that’s what my colleagues tell me,” says Rajewsky.
“Since octopuses are not typical model organisms, our molecular biological tools were very limited,” says Zolotarov. “So we don’t yet know exactly which cell types express the new microRNAs.” Rajewski’s team now plans to apply a technique developed in Rajewski’s lab that makes cells in octopus tissue visible at a molecular level.
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Original Research: open access.
🇧🇷MicroRNAs are deeply involved in the formation of the complex octopus brain” Nikolaus Rajewsky et al. Advances in science
MicroRNAs are deeply involved in the formation of the complex octopus brain
Soft-bodied cephalopods, such as octopuses, are highly intelligent invertebrates with highly complex nervous systems that evolved independently of vertebrates. Because of the high RNA editing in their neural tissues, we hypothesized that RNA regulation may play a major role in the cognitive success of this group.
Thus, we profiled messenger RNAs and small RNAs in three cephalopod species including 18 tissues. octopus vulgaris🇧🇷 We show that the main RNA innovation of soft-bodied cephalopods is the expansion of the microRNA (miRNA) gene repertoire.
Through this evolutionary pathway, new miRNAs were primarily expressed and conserved in mature neuronal tissues and during development, and thus have putative functional target sites. The only comparable miRNA expansions have occurred, particularly in vertebrates.
Thus, we propose that miRNAs are closely related to the evolution of complex animal brains.