The origin of hearing in humans is connected with the sense of touch of sea anemones.

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Behind the seeming simplicity – a cylinder topped with tentacles – an anemone hides great complexity. It is noticeably closer to us than we might think, its genome is very similar to ours. These similarities make sea anemones an ideal model for studying the animal genome and understanding the interactions between genes. Recently, an international team of researchers discovered a touch-related developmental gene in sea anemone tentacles that is already known to be involved in hearing development in humans. This discovery shows a genetic link between the two species, suggesting a common ancestor and evolutionary history of hearing in humans.

In 2007, a group of American researchers unexpectedly discovered that the genome of the anemone, which belongs to the same category as corals and jellyfish, the first divergent branch of multicellular animals, more closely resembles the genome of humans and other vertebrates than the genome of classical laboratory models such as fruit flies and worms. -nematodes. The latter would have lost a number of genes from common ancestors that would have retained sea anemones and vertebrates.

The anemone genome, which is more similar, provides a good benchmark for comparison with the human genome in order to find the genes of our common ancestor and their organization on chromosomes. Heather Marlowe, Developmental Biologist in the Department of Vertebrate Developmental Genomics and Epigenomics at the Pasteur Institute, explains: “ When the sea anemone’s genome was sequenced in 2007, it was found to be very similar to the human one in both number of genes (about 20,000 genes) and organization. These similarities make sea anemones an ideal model for studying the animal genome and understanding the interactions between genes. “.

In addition, the sea anemone occupies a strategic position on the tree of life. The evolutionary branch of cnidarians to which anemones belong separated from bilaterals, in other words, from most other animals, including humans, more than 600 million years ago. Heather Marlow summarizes: ” In this way, sea anemones can also help us understand the origin and evolution of the many types of cells that make up the bodies and organs of animals, and in particular their nervous systems. “. In 2018, the same team identified a very complex nervous and sensory system with almost thirty different types of neurons – peptidergic, glutamatergic, or even insulinergic.

In this context, an international team led by biologist Ethan Ozment of the University of Arkansas recently published an article in the journal electronic lifereporting the discovery of a developmental gene associated with touch in sea anemone tentacles, which is also known to be associated with hearing in humans.

Sensory cells of common origin

One of the most fundamental types of sensory cells that emerged in the course of animal evolution is the mechanosensory cell. This is a specialized sensory epithelial cell that converts mechanical stimuli – for example, water vibrations, skin pressure, stretching, etc. – into internal signals. These signals are then transmitted, usually via the nervous system, to effector cells, such as muscle cells, to elicit behavioral and/or physiological responses in the body. This is a mechanoreceptor.

Despite this place in animal phylogeny, the earliest evolutionary histories of mechanoreceptor development remain enigmatic. We know that the classic type of mechanosensory cell with a special sensory-neuronal function, i.e., generating a nerve impulse when the adjacent tissue is deformed, is a hair cell. Moreover, in humans and other vertebrates, sensory receptors in the auditory system are equipped with them. These cells have bundles of finger-shaped organelles called stereocilia that pick up mechanical stimuli, that is, vibrations that we hear as sound.

As mentioned above, sea anemones are a more appropriate model for studying the history of human evolution because traits shared by bilateral animals and cnidarians were likely present in our last common ancestor. Indeed, these sea anemones belong to the Cnidaria group, sister group bilateria including vertebrates. These two groups diverged from their last common ancestor, who lived from 748 to 604 million years ago. In addition, sea anemones also possess hair cells with morphological and functional characteristics similar to those of mechanosensory cells in other animal lines. Unfortunately, no research has looked at the genes needed to develop these cnidarian hair cells, which could tell us about our evolutionary history.

To clarify these questions, the investigators of the present study drew on previous work that had revealed the existence of a specific gene, the POU-IV gene. The latter is inherent in all existing groups of animals, with the exception of ctenophores, indicating an early appearance in animal evolution. Its participation in the development of ciliated cells in mammals is confirmed by experiments on mice. The latter, if they lack the POU-IV gene, are deaf. However, its role in the sensory development of the sea anemone and its evolution in animal phylogeny remained unknown.

The gene responsible for hearing and touch

To understand what the POU-IV gene does in the star anemone (Nematostella vectensis), the team disabled it using the CRISPR-Cas9 gene editing tool. To do this, the researchers injected a mixture containing the Cas9 protein into fertilized sea anemone eggs to knock out the gene, and studied developing embryos as well as cultured mutated sea anemones.

They then discovered that deleting the gene resulted in abnormal hair cell development. Indeed, the mutant anemones exhibited aberrant hair cell growth and lack of sensitivity to touch compared to wild-type control anemones. In other words, without the POU-IV gene, they couldn’t perceive physical stimuli through their hair cells.

Behavior of wild-type (F2 POU-IV +/+, A, B) and mutant (F2 POU-IV -/-, C, D) anemones in response to tactile stimuli of their oral tentacles. Animals are shown before (A, C) and after (B, D) touching the tentacles. Tactile tentacle stimuli cause wild-type tentacles to retract at the ends of arrows. © E. Ozment et al., 2022

In addition, the mutant anemones strongly repressed a gene very similar to the polycystin 1 gene, which is required for the normal perception of fluid flow by vertebrate kidney cells. The sense of fluid flow can be a useful feature for aquatic organisms, even though sea anemones do not have buds.

Taken together, the results suggest that POU-IV may have played a role in the evolution of mechanoreceptor cells in a single ancestor of cnidarians and bilaterians. This is stated in the statement of the researchers: This study is interesting because it not only opens up a new area of ​​research into how mechanosensing develops and functions in sea anemones, but also informs us that the building blocks of our hearing have evolutionary roots dating back hundreds of millions of years. years before the Precambrian. The early role of POU-IV in mechanoreceptor differentiation in animal evolution remains unresolved and requires comparative data on placozoans and sponges. “.

The results of this work open up an entirely new area of ​​research into the development and functions of mechanoreception in cnidarians. In addition, this discovery indicates that the evolution of our hearing has a very ancient history. It will be necessary to use information from other types with older divergences to trace the history of the gene even further.

Ultimately, the researchers plan to study the mechanism by which POU-IV activates different sets of genes in cnidocytes and hair cells to shed light on how POU-IV may have contributed to the evolution of a new type of mechanosensory cell. Cnidaria.

Source: eLife

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