Tardigrades have recovered genes from extinct species to become (almost) indestructible

Imagine a very small organism present everywhere on our planet around us and which carries with it a lost genetic memory. Tardigrades are invertebrates measuring 0.2 to 1.2 millimeters maximum that resemble mini bear cubs with four pairs of legs, muscles, neurons and a microbiota. They can be found everywhere on our planet, from the ocean floors to the summit of the Himalayas.

Tardigrades are also called water bears, because they always live in an environment where water is present such as oceans, glaciers, rivers or in the gutters of houses, but also in mosses and lichens on trees. or rocks. We already know nearly 1,500 species: they are the champions of the survival of our planet and the undisputed kings of a very select club called extremophiles, these organisms capable of surviving the most extreme environments.

Indeed, tardigrades are capable of withstanding the lowest temperature measured in the universe (-272°C) or even heat close to that measured on the planet Mercury (+151°C). They even manage to survive at a temperature close to absolute zero (-273.16°C), which does not exist in the universe but only in physics laboratories. In a recent physics experiment, one individual out of three tardigrades of the species Ramazzotius varieornatus, photographed below, was successfully resuscitated after exposure to a temperature close to absolute zero.

Tardigrades can also survive a ten-day stay in the vacuum of space exposed directly to cosmic rays and have become a working model for astrobiology research. On the radiation side, we know that they can survive doses of X-rays 1,000 times higher than fatal doses for humans. Their resistance to gigantic pressures has also been tested for several hours and, surprisingly, they survive being crushed by the weight equivalent to a building of… 60,000 floors.

Cryptobiosis: life suspended

A first discovery of tardigrades dates back to the 18th century^e century. After studying with the Jesuits of Reggio (Calabria, Italy), the biologist and philosopher Lazzaro Spallanzani (1729-1799) published in 1776 a first study on these small animals in his work Booklets on animal and plant physics. He gives them the name tardigrade and observes their ability to be able to dehydrate completely and then “resurrect after death” in the presence of water and describe, for the first time, the phenomenon of cryptobiosis.

Cryptobiosis is a “state of suspended life” during which no indicators of life are detectable. In this state, tardigrades collected in Antarctica were successfully awakened after thirty years. Other data showed that tardigrades in cryptobiosis are in a “state of suspended life” but also “out of time.” In fact, the time spent in this state of cryptobiosis is not deducted from their normal lifespan (the average lifespan of a species of tardigrade in controlled breeding is approximately 60 days). In short, whether it enters cryptobiosis or not, a tardigrade will not see its normal active life expectancy modified. The Anglo-Saxons call this phenomenon «Sleeping Beauty» or “Sleeping Beauty”indicating that an organism stops aging as long as it remains in this state.

Our CNRS laboratory in Montpellier was the first to successfully observe what happens inside a species of tardigrade (Hypsibius exemplaris) when it enters cryptobiosis. In this state, this species miniaturizes, losing 38% of its volume and creates a sort of visible rampart around each of the cells that make up its body. This structure gradually disappears during resuscitation of the animal.

Survival strategies that differ depending on the species

But the most surprising comes from a recent study by our laboratory concerning a species related to the first (Ramazzottius varieornatus) also from our farms. When it enters cryptobiosis, this species only miniaturizes by 32%. Even more surprising: it was impossible to observe the presence of this specific rampart of cryptobiosis which surrounded the cells of the previous species. These experiments indicate that different species of tardigrades are capable of withstanding stresses that are fatal to other living species, but that they do so in different ways and using tools that are not all common to them.

From 2016, this set of genetic tools allowing them to resist extreme environments began to be identified during the first sequencing of their genomes. These tools are already of interest to scientists for future revolutionary biomedical applications such as the preservation of drugs and vaccines in a dehydrated form, or the protection of cells against deadly radiation which would be useful for future space missions.

Geneticists believe that these genes were acquired by tardigrades to allow them to resist dehydration, but they also propose that it is these same genetic tools that allow them to resist all types of deadly environments. By studying their genetic makeup, scientists were surprised to observe that nearly 40% of tardigrade genes are unknown in other species currently living on our planet.

But where do these genes called “unique tardigrade genes” come from? One explanation involves the mechanism of horizontal gene transfer (or HGT, for «Horizontal Gene Transfert»). As shown below, a living organism typically inherits genes from its parents vertically.

Acquire genes from your neighbors

In the case of horizontal gene transfer, the organism has an additional option which is the ability to acquire genes from its neighbors and retain them if they prove advantageous for the survival of its species. This has already been observed in a species of aphid in which the green individuals are eaten by ladybugs while the red ones are parasitized by wasps. An aphid had the “good idea” of acquiring a fungus gene by horizontal gene transfer and adopting a yellow color which protects it very effectively against these two predators.

More recently, the study of a new species of tardigrade identified in China revealed that it had acquired the gene from a species of bacteria allowing it to protect itself against lethal doses of X-rays. For these two examples, the The organism responsible for this genetic gift has been identified because it is still alive, but for the unique tardigrade genes this is not possible.

It would seem that tardigrades, which have inhabited our planet for around 600 million years, have had time to acquire numerous genes by horizontal transfer from species that are now extinct to build up a veritable library. This is all the more possible given that tardigrades have resisted the five major extinctions of living species that our planet has experienced during its history, the most recent having taken away the dinosaurs. A small number of these unique tardigrade genes have already been identified and given bizarre names such as Dsup, TDR1, CAHS, SAHS, MAHS, TDPs, LEA, Doda1 or Trid1.

Placed in human cells or other laboratory organisms (drosophila, bacteria, yeast, plants, etc.), these genes were able to increase their resistance spectacularly to normally fatal treatments such as X-rays, ultraviolet or strong oxidants. Better still, proteins from some of these genes have been able to protect drugs from dehydration and thus allow their storage at room temperature, thus revealing enormous potential for the distribution of vaccines without the need for expensive freezers.

The future use of these unique tardigrade genes in the biomedical field is already the subject of numerous patent filings, heralding new revolutionary biomedical technologies that could soon result. These range from protecting the skin of astronauts against cosmic rays to the possibility of preserving medicines, tissues or organs awaiting use by dehydration.

A “scent of DNA”

But where do these DNAs that can be incorporated by tardigrades come from? The answer lies around us. We are constantly bathed in a “scent of DNA” released by all living organisms around us. This DNA is called eDNA, for environmental DNA. A soil sample can make it possible, after sequencing the DNA it contains, to determine which living species live in a given place, even without having seen them. This is a very effective technique for assessing the biodiversity of a terrestrial or marine environment. Recently, scientists successfully identified the DNA signature of Asian elephants and giraffes from samples taken from a spider web nearly 195 meters away in the Perth Zoo in Australia.

The scientists imagined a possible scenario to explain how these pieces of eDNA can be found in species of tardigrades, as well as in certain worms or some other invertebrates. These organisms all share the ability to survive more or less prolonged dehydration. When they are in cryptobiosis after dehydration, we observe the progressive appearance of breaks in their chromosomes.

Tardigrades will be able to repair this damage as soon as they rehydrate. Water is potentially capable of transporting fragments of eDNA to the nucleus of cells where the chromosomes are located. Their presence among the fragmented chromosomes of tardigrades makes it possible to envisage the possible integration of these at the same time as the repair mechanisms are at work.

With their power to capture new genes present in their environment, tardigrades have accumulated genes with exceptional properties from species that have long since disappeared from our planet. These unique tardigrade genes perhaps contain the secrets of future biomedical revolutions by offering new possibilities of protection and transport for drugs and fragile tissues, new protections for future missions already planned by space agencies or even in dermocosmetics for combat the effects of age.

Simon Galas is professor of genetics and molecular biology of aging at the Faculty of Pharmacy of the University of Montpellier. Myriam Richaud is a doctor in genetics and molecular biology of aging at the Faculty of Pharmacy of the University of Montpellier.

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