Environmental tolerance in tardigrades

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When dried, terrestrial tardigrades draw in their legs and go into a 'tun' state. They can quickly revive when re-wetted.
mg = midgut; go = gonad;
pb = pharyngeal bulb; mo = mouth; st = stylet Tardigrade anhydrobiosis cycle.svg
When dried, terrestrial tardigrades draw in their legs and go into a 'tun' state. They can quickly revive when re-wetted.
mg = midgut; go = gonad;
pb = pharyngeal bulb; mo = mouth; st = stylet

From the early 19th century, tardigrades' environmental tolerance has been a noted feature of the group. The animals are able to survive extremes of temperature, desiccation, impact, radiation, and exposure to the vacuum of space.

Contents

Environmental tolerance

In 1834, C.A.S. Schulze, giving the first formal description of a tardigrade, Macrobiotus hufelandi, explicitly noted the animal's exceptional ability to tolerate environmental stress, subtitling his work "a new animal from the crustacean class, capable of reviving after prolonged asphyxia and dryness". [2] [3]

Tardigrades are not considered extremophilic because they are not adapted to exploit extreme conditions, only to endure them. This means that their chances of dying increase the longer they are exposed to the extreme environments, [4] whereas true extremophiles thrive there. [5]

Cryptobiosis and the dehydrated 'tun' state

Video of anhydrobiosis, a form of cryptobiosis, in the tardigrade Richtersius coronifer

Tardigrades are capable of suspending their metabolism, going into a state of cryptobiosis. [1] Terrestrial and freshwater tardigrades are able to tolerate long periods when water is not available, such as when the moss or pond they are living in dries out, by drawing their legs in and forming a desiccated cyst, the cryptobiotic 'tun' state, where no metabolic activity takes place. [1] In this state, they can go without food or water for several years. [1] Further, in that state they become highly resistant to environmental stresses, including temperatures from as low as −272 °C (−458 °F) to as much as +149 °C (300 °F) (at least for short periods of time [6] ), lack of oxygen, [1] vacuum, [1] ionising radiation, [1] [7] and high pressure. [8]

Marine tardigrades such as Halobiotus crispae alternate each year (cyclomorphosis) between an active summer morph and a hibernating winter morph (a pseudosimplex) that can resist freezing and low salinity, but which remains active throughout. Reproduction however takes place only in the summer morph. [1]

Specific environmental stresses

Extremes of temperature

Tardigrades can survive in extremes of temperature that would kill almost any other animal, including: [9] [10] [11]

Tardigrades are however sensitive to high temperatures: 48 hours at 37.1 °C (98.8 °F) kills half of unacclimitized active tardigrades. Acclimation boosts the lethal temperature to 37.6 °C (99.7 °F). Those in the tun state fare better, half surviving 82.7 °C (180.9 °F) for one hour. Longer exposure decreases the lethal temperature. For 24 hours of exposure, 63.1 °C (145.6 °F) kills half of the tun state tardigrades. [15]

Impact

Tardigrades can survive impacts up to about 900 metres per second (3,000 ft/s), and momentary shock pressures up to about 1.14 gigapascals (165,000 psi). [16]

Radiation

Tardigrades can withstand 1,000 times more radiation than other animals, [17] median lethal doses of 5,000 Gy (of gamma rays) and 6,200 Gy (of heavy ions) in hydrated animals (5 to 10 Gy could be fatal to a human). [18] Earlier experiments attributed this to their lowered water content, providing fewer reactants for ionizing radiation. [18] However, tardigrades, when hydrated, remain much more resistant to shortwave UV radiation than other animals; one reason is their ability to repair damage to their DNA. [19]

Exposure to space

The 2007 FOTON-M3 mission carrying the BIOPAN astrobiology payload (illustrated) exposed tardigrades to vacuum, solar ultraviolet, or both, showing their ability to survive in the space environment. Biopan Space Expo 001.jpg
The 2007 FOTON-M3 mission carrying the BIOPAN astrobiology payload (illustrated) exposed tardigrades to vacuum, solar ultraviolet, or both, showing their ability to survive in the space environment.

Tardigrades have survived exposure to space. In 2007, dehydrated tardigrades were taken into low Earth orbit on the FOTON-M3 mission carrying the BIOPAN astrobiology payload. For 10 days, groups of tardigrades, some of them previously dehydrated, some of them not, were exposed to the hard vacuum of space, or vacuum and solar ultraviolet radiation. [20] Back on Earth, more than 68% of the subjects protected from solar ultraviolet radiation were reanimated within 30 minutes following rehydration; although subsequent mortality was high, many produced viable embryos. [20]

In contrast, hydrated samples exposed to the combined effect of vacuum and full solar ultraviolet radiation had significantly reduced survival, with only three subjects of Milnesium tardigradum surviving. [20] The space vacuum did not much affect egg-laying in either R. coronifer or M. tardigradum, whereas UV radiation did reduce egg-laying in M. tardigradum. [21] In 2011, Italian scientists sent tardigrades on board the International Space Station along with extremophiles on STS-134. [22] They concluded that microgravity and cosmic radiation "did not significantly affect survival of tardigrades in flight" and that tardigrades could be useful in space research. [23] [24]

In 2019, a capsule containing tardigrades in a cryptobiotic state was on board the Israeli lunar lander Beresheet which crashed on the Moon; they were described as unlikely to have survived the impact. [16] Despite tardigrades' ability to survive in space, tardigrades on Mars would still need food. [25]

Damage protection proteins

Tardigrades' ability to remain desiccated for long periods of time was thought to depend on high levels of the sugar trehalose, [26] common in organisms that survive desiccation. [9] However, tardigrades do not synthesize enough trehalose for this function. [26] Instead, tardigrades produce intrinsically disordered proteins in response to desiccation. Three of these are specific to tardigrades and have been called tardigrade specific proteins. These may protect membranes from damage by associating with the polar heads of lipid molecules. [27] The proteins may also form a glass-like matrix that protects cytoplasm from damage during desiccation. [28] Anhydrobiosis in response to desiccation has a complex molecular basis; in Hypsibius exemplaris , 1,422 genes are upregulated during the process. Of those, 406 are specific to tardigrades, 55 being intrinsically disordered and the others globular with unknown functions. [29]

Tardigrades possess a cold shock protein; Maria Kamilari and colleagues propose (2019) that this may serve "as a RNA-chaperone involved in regulation of translation [of RNA code to proteins] following freezing." [9]

Tardigrade DNA is protected from radiation by the Dsup ("damage suppressor") protein. [30] The Dsup proteins of Ramazzottius varieornatus and H. exemplaris promote survival by binding to nucleosomes and protecting chromosomal DNA from hydroxyl radicals. [31] The Dsup protein of R. varieornatus confers resistance to ultraviolet-C by upregulating DNA repair genes. [32]

Related Research Articles

<span class="mw-page-title-main">Extremophile</span> Organisms capable of living in extreme environments

An extremophile is an organism that is able to live in extreme environments, i.e., environments with conditions approaching or stretching the limits of what known life can adapt to, such as extreme temperature, pressure, radiation, salinity, or pH level.

Radioresistance is the level of ionizing radiation that organisms are able to withstand.

<span class="mw-page-title-main">Cryptobiosis</span> Metabolic state of life

Cryptobiosis or anabiosis is a metabolic state in extremophilic organisms in response to adverse environmental conditions such as desiccation, freezing, and oxygen deficiency. In the cryptobiotic state, all measurable metabolic processes stop, preventing reproduction, development, and repair. When environmental conditions return to being hospitable, the organism will return to its metabolic state of life as it was prior to cryptobiosis.

<span class="mw-page-title-main">EXPOSE</span> External facility on the ISS dedicated to astrobiology experiments

EXPOSE is a multi-user facility mounted outside the International Space Station (ISS) dedicated to astrobiology. EXPOSE was developed by the European Space Agency (ESA) for long-term spaceflights and was designed to allow exposure of chemical and biological samples to outer space while recording data during exposure.

<span class="mw-page-title-main">Eurytherm</span> Organism tolerant of a wide temperature range

A eurytherm is an organism, often an endotherm, that can function at a wide range of ambient temperatures. To be considered a eurytherm, all stages of an organism's life cycle must be considered, including juvenile and larval stages. These wide ranges of tolerable temperatures are directly derived from the tolerance of a given eurythermal organism's proteins. Extreme examples of eurytherms include Tardigrades (Tardigrada), the desert pupfish, and green crabs, however, nearly all mammals, including humans, are considered eurytherms. Eurythermy can be an evolutionary advantage: adaptations to cold temperatures, called cold-eurythemy, are seen as essential for the survival of species during ice ages. In addition, the ability to survive in a wide range of temperatures increases a species' ability to inhabit other areas, an advantage for natural selection.

<span class="mw-page-title-main">Tardigrade</span> Phylum of microscopic animals

Tardigrades, known colloquially as water bears or moss piglets, are a phylum of eight-legged segmented micro-animals. They were first described by the German zoologist Johann August Ephraim Goeze in 1773, who called them Kleiner Wasserbär'little water bear'. In 1776, the Italian biologist Lazzaro Spallanzani named them Tardigrada, which means 'slow walker'.

Polypedilum vanderplanki or the sleeping chironomid, is a dipteran in the family Chironomidae. It occurs in the semi-arid regions of the African continent. Its larvae are found in small tubular nests in the mud at the bottom of temporary pools that frequently dry out during the lifetime of P. vanderplanki larvae. Under these conditions, the larvae's body desiccates to as low as 3% water content by weight. In the dehydrated state the larvae become impervious to many extreme environmental conditions, and can survive temperatures from 3 K to up to 375 K, very high levels of gamma-rays, and exposure to vacuum. It is one of few metazoans that can withstand near complete desiccation (anhydrobiosis) in order to survive adverse environmental conditions. Slow desiccation enabled larvae to synthesize 38 μg trehalose/individual, and all of them recovered after rehydration, whereas larvae that were dehydrated 3 times faster accumulated only 6.8 μg trehalose/individual and none of them revived after rehydration. Late Embryo Abundant (LEA), anti-oxidant, and heat-shock proteins may also be involved in survival. This species is considered the most cold-tolerant insect species, able to survive liquid helium (−270 °C) exposure for up to 5 min. with a 100% survival rate when desiccated to 8% water content.

<i>Deinococcus radiodurans</i> Radioresistant extremophile species of bacterium

Deinococcus radiodurans is a bacterium, an extremophile and one of the most radiation-resistant organisms known. It can survive cold, dehydration, vacuum, and acid, and therefore is known as a polyextremophile. The Guinness Book Of World Records listed it in January 1998 as the world's most radiation-resistant bacterium or lifeform. However the archaea Thermococcus gammatolerans is actually the most resistant organism to radiation.

<i>Hypsibius dujardini</i> Species of tardigrade

Hypsibius dujardini sensu lato is a species complex of tardigrade in the class Eutardigrada. A member of this complex, Hypsibius exemplaris, is widely used for various research projects pertaining to evolutionary biology and astrobiology. The species was described by Louis Michel François Doyère in 1840.

<i>Ramazzottius</i> Genus of tardigrades

Ramazzottius is a genus of water bear or moss piglet, a tardigrade in the class Eutardigrada, named after the Italian zoologist Giuseppe Ramazzotti.

<i>Acutuncus</i> Genus of tardigrades

Acutuncus is a genus of tardigrades containing a single species, Acutuncus antarcticus. Tardigrades, which are eight-legged micro-animals, are commonly referred to as water bears or moss piglets and are found all over the world in varying extreme habitats. First discovered in 1904 and originally named Hypsibius antarcticus, Acutuncus antarcticus is the most abundant tardigrade species in Antarctica.

<i>Chroococcidiopsis</i> Genus of bacteria

Chroococcidiopsis is a photosynthetic, coccoidal bacterium, and the only genus in the order Chroococcidiopsidales and in the family Chroococcidiopsidaceae. A diversity of species and cultures exist within the genus, with a diversity of phenotypes. Some extremophile members of Chroococcidiopsis are known for their ability to survive harsh environmental conditions, including both high and low temperatures, ionizing radiation, and high salinity.

<i>Milnesium tardigradum</i> Species of tardigrade

Milnesium tardigradum is a cosmopolitan species of tardigrade that can be found in a diverse range of environments. It has also been found in the sea around Antarctica. M. tardigradum was described by Louis Michel François Doyère in 1840. It contains unidentified osmolytes that could potentially provide important information in the process of cryptobiosis.

<i>Milnesium</i> Genus of tardigrades

Milnesium is a genus of tardigrades. It is rather common, being found in a wide variety of habitats across the world. It has a fossil record extending back to the Cretaceous, the oldest species found so far is known from Turonian stage deposits on the east coast of the United States. Milnesiums are one of the most desiccation and radiation-resistant invertebrates on Earth because of their unique ability to transform into a "tun" state and utilize intrinsically disordered proteins when experiencing extreme environments.

Dsup is a DNA-associating protein, unique to the tardigrade, that suppresses the occurrence of DNA breaks by radiation. When human HEK293 cells were engineered with Dsup proteins, they showed approximately 40% more tolerance against X-ray radiation.

Tardigrade specific proteins are types of intrinsically disordered proteins specific to tardigrades. These proteins help tardigrades survive desiccation, one of the adaptations which contribute to tardigrade's extremotolerant nature. Tardigrade specific proteins are strongly influenced by their environment, leading to adaptive malleability across a variety of extreme abiotic environments.

<i>Milnesium alpigenum</i> Species of tardigrade

Milnesium alpigenum is a species of tardigrade that falls under the Tardigrada phylum. Like its taxonomic relatives it is an omnivorous predator that feeds on other small organisms, such as algae, rotifers, and nematodes. M. alpigenum was discovered by Christian Gottfried Ehrenberg in 1853. It is very closely related to Milnesium tardigradum along with many other species from the Milnesium genus.

<span class="mw-page-title-main">Tardigrades on the Moon</span> Possibly lunar-lander-crash-surviving tardigrades

On April 11, 2019, the Israeli spacecraft Beresheet crashed into the Moon during a failed landing attempt. Its payload included a few thousand tardigrades. Initial reports suggested they could have survived the crash landing. If any of them did survive, they would be the tenth species to reach the surface of the Moon, after humans, brought by the American Apollo program, and fruit flies, silkworms, cottonseed, potato, rapeseed, Arabidopsis thaliana, as well as yeast — the latter seven all taken to the moon by China's Chang'e 4.

We believe the chances of survival for the tardigrades... are extremely high.

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