Cryptobiosis

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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.

Contents

Forms

Anhydrobiosis

Anhydrobiosis in the tardigrade Richtersius coronifer

Anhydrobiosis is the most studied form of cryptobiosis and occurs in situations of extreme desiccation. The term anhydrobiosis derives from the Greek for "life without water" and is most commonly used for the desiccation tolerance observed in certain invertebrate animals such as bdelloid rotifers, tardigrades, brine shrimp, nematodes, and at least one insect, a species of chironomid ( Polypedilum vanderplanki ). However, other life forms exhibit desiccation tolerance. These include the resurrection plant Craterostigma plantagineum , [1] the majority of plant seeds, and many microorganisms such as bakers' yeast. [2] Studies have shown that some anhydrobiotic organisms can survive for decades, even centuries, in the dry state. [3]

Invertebrates undergoing anhydrobiosis often contract into a smaller shape and some proceed to form a sugar called trehalose. Desiccation tolerance in plants is associated with the production of another sugar, sucrose. These sugars are thought to protect the organism from desiccation damage. [4] In some creatures, such as bdelloid rotifers, no trehalose has been found, which has led scientists to propose other mechanisms of anhydrobiosis, possibly involving intrinsically disordered proteins. [5]

In 2011, Caenorhabditis elegans , a nematode that is also one of the best-studied model organisms, was shown to undergo anhydrobiosis in the dauer larva stage. [6] Further research taking advantage of genetic and biochemical tools available for this organism revealed that in addition to trehalose biosynthesis, a set of other functional pathways is involved in anhydrobiosis at the molecular level. [7] These are mainly defense mechanisms against reactive oxygen species and xenobiotics, expression of heat shock proteins and intrinsically disordered proteins as well as biosynthesis of polyunsaturated fatty acids and polyamines. Some of them are conserved among anhydrobiotic plants and animals, suggesting that anhydrobiotic ability may depend on a set of common mechanisms. Understanding these mechanisms in detail might enable modification of non-anhydrobiotic cells, tissues, organs or even organisms so that they can be preserved in a dried state of suspended animation over long time periods.

As of 2004, such an application of anhydrobiosis is being applied to vaccines. In vaccines, the process can produce a dry vaccine that reactivates once it is injected into the body. In theory, dry-vaccine technology could be used on any vaccine, including live vaccines such as the one for measles. It could also potentially be adapted to allow a vaccine's slow release, eliminating the need for boosters. This proposes to eliminate the need for refrigerating vaccines, thus making dry vaccines more widely available throughout the developing world where refrigeration, electricity, and proper storage are less accessible. [8]

Based on similar principles, lyopreservation has been developed as a technique for preservation of biological samples at ambient temperatures. [9] [10] Lyopreservation is a biomimetic strategy based on anhydrobiosis to preserve cells at ambient temperatures. It has been explored as an alternative technique for cryopreservation. The technique has the advantages of being able to preserve biological samples at ambient temperatures, without the need for refrigeration or use of cryogenic temperatures. [11] [12]

Anoxybiosis

SEM image of Milnesium tardigradum in tun state - journal.pone.0045682.g001-3.png
SEM image of Milnesium tardigradum in tun (suspended) state
SEM image of Milnesium tardigradum in active state - journal.pone.0045682.g001-2.png
SEM image of Milnesium tardigradum in active state

In situations lacking oxygen (a.k.a., anoxia), many cryptobionts (such as M. tardigradum) take in water and become turgid and immobile, but can survive for prolonged periods of time. Some ectothermic vertebrates and some invertebrates, such as brine shrimps, [13] copepods, [14] nematodes, [15] and sponge gemmules, [16] are capable of surviving in a seemingly inactive state during anoxic conditions for months to decades.

Studies of the metabolic activity of these idling organisms during anoxia have been mostly inconclusive. This is because it is difficult to measure very small degrees of metabolic activity reliably enough to prove a cryptobiotic state rather than ordinary metabolic rate depression (MRD). Many experts are skeptical of the biological feasibility of anoxybiosis, as the organism is managing to prevent damage to its cellular structures from the environmental negative free energy, despite being both surrounded by plenty of water and thermal energy and without using any free energy of its own. However, there is evidence that the stress-induced protein p26 may act as a protein chaperone that requires no energy in cystic Artemia franciscana (sea monkey) embryos, and most likely an extremely specialized and slow guanine polynucleotide pathway continues to provide metabolic free energy to the A. franciscana embryos during anoxic conditions. It seems that A. franciscana approaches but does not reach true anoxybiosis. [17]

Chemobiosis

Chemobiosis is the cryptobiotic response to high levels of environmental toxins. It has been observed in tardigrades. [18]

Cryobiosis

Cryobiosis is a form of cryptobiosis that takes place in reaction to decreased temperature. Cryobiosis begins when the water surrounding the organism's cells has been frozen. Stopping molecule mobility allows the organism to endure the freezing temperatures until more hospitable conditions return. Organisms capable of enduring these conditions typically feature molecules that facilitate freezing of water in preferential locations while also prohibiting the growth of large ice crystals that could otherwise damage cells.[ citation needed ] One such organism is the lobster. [19]

Osmobiosis

Osmobiosis is the least studied of all types of cryptobiosis. Osmobiosis occurs in response to increased solute concentration in the solution the organism lives in. Little is known for certain, other than that osmobiosis appears to involve a cessation of metabolism. [18]

Examples

The brine shrimp Artemia salina, which can be found in the Makgadikgadi Pans in Botswana, [20] survives over the dry season when the water of the pans evaporates, leaving a virtually desiccated lake bed.

The tardigrade, or water bear, can undergo all five types of cryptobiosis. While in a cryptobiotic state, its metabolism reduces to less than 0.01% of what is normal, and its water content can drop to 1% of normal. [21] It can withstand extreme temperature, radiation, and pressure while in a cryptobiotic state. [22]

Some nematodes and rotifers can also undergo cryptobiosis. [23]

See also

Related Research Articles

Biostasis or Cryptobiosis is the ability of an organism to tolerate environmental changes without having to actively adapt to them. Biostasis is found in organisms that live in habitats that likely encounter unfavorable living conditions, such as drought, freezing temperatures, change in pH levels, pressure, or temperature. Insects undergo a type of dormancy to survive these conditions, called diapause. Diapause may be obligatory for these insects to survive. The insect may also be able to undergo change prior to the arrival of the initiating event.

<span class="mw-page-title-main">Rotifer</span> Phylum of pseudocoelomate invertebrates

The rotifers, commonly called wheel animals or wheel animalcules, make up a phylum of microscopic and near-microscopic pseudocoelomate animals.

<span class="mw-page-title-main">Bdelloidea</span> Class of parthenogenetic freshwater rotifers

Bdelloidea is a class of rotifers found in freshwater habitats all over the world. There are over 450 described species of bdelloid rotifers, distinguished from each other mainly on the basis of morphology. The main characteristics that distinguish bdelloids from related groups of rotifers are exclusively parthenogenetic reproduction and the ability to survive in dry, harsh environments by entering a state of desiccation-induced dormancy (anhydrobiosis) at any life stage. They are often referred to as "ancient asexuals" due to their unique asexual history that spans back to over 25 million years ago through fossil evidence. Bdelloid rotifers are microscopic organisms, typically between 150 and 700 µm in length. Most are slightly too small to be seen with the naked eye, but appear as tiny white dots through even a weak hand lens, especially in bright light. In June 2021, biologists reported the restoration of bdelloid rotifers after being frozen for 24,000 years in the Siberian permafrost.

<span class="mw-page-title-main">Desiccation</span> State of extreme dryness or process of thorough drying

Desiccation is the state of extreme dryness, or the process of extreme drying. A desiccant is a hygroscopic substance that induces or sustains such a state in its local vicinity in a moderately sealed container.

<span class="mw-page-title-main">Trehalose</span> Chemical compound

Trehalose is a sugar consisting of two molecules of glucose. It is also known as mycose or tremalose. Some bacteria, fungi, plants and invertebrate animals synthesize it as a source of energy, and to survive freezing and lack of water.

<span class="mw-page-title-main">Microbial cyst</span> Resting or dormant stage of a microorganism

A microbial cyst is a resting or dormant stage of a microorganism, usually a bacterium or a protist or rarely an invertebrate animal, that helps the organism to survive in unfavorable environmental conditions. It can be thought of as a state of suspended animation in which the metabolic processes of the cell are slowed and the cell ceases all activities like feeding and locomotion. Encystment, the formation of the cyst, also helps the microbe to disperse easily, from one host to another or to a more favorable environment. When the encysted microbe reaches an environment favorable to its growth and survival, the cyst wall breaks down by a process known as excystation. In excystment, the exact stimulus is unknown for most protists.

<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.

Osmoprotectants or compatible solutes are small organic molecules with neutral charge and low toxicity at high concentrations that act as osmolytes and help organisms survive extreme osmotic stress. Osmoprotectants can be placed in three chemical classes: betaines and associated molecules, sugars and polyols, and amino acids. These molecules accumulate in cells and balance the osmotic difference between the cell's surroundings and the cytosol. In plants, their accumulation can increase survival during stresses such as drought. In extreme cases, such as in bdelloid rotifers, tardigrades, brine shrimp, and nematodes, these molecules can allow cells to survive being completely dried out and let them enter a state of suspended animation called cryptobiosis.

<span class="mw-page-title-main">Tardigrade</span> Phylum of microscopic animals, also known as water bears

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. In 1777, the Italian biologist Lazzaro Spallanzani named them Tardigrada, which means "slow steppers".

Desiccation tolerance refers to the ability of an organism to withstand or endure extreme dryness, or drought-like conditions. Plants and animals living in arid or periodically arid environments such as temporary streams or ponds may face the challenge of desiccation, therefore physiological or behavioral adaptations to withstand these periods are necessary to ensure survival. In particular, insects occupy a wide range of ecologically diverse niches and, so, exhibit a variety of strategies to avoid desiccation.

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.

<span class="mw-page-title-main">Antarctic microorganism</span>

Antarctica is one of the most physically and chemically extreme terrestrial environments to be inhabited by lifeforms. The largest plants are mosses, and the largest animals that do not leave the continent are a few species of insects.

Late embryogenesis abundant proteins are proteins in plants, and some bacteria and invertebrates, that protect against protein aggregation due to desiccation or osmotic stresses associated with low temperature. LEA proteins were initially discovered accumulating late in embryogenesis of cotton seeds. Although abundant in seeds and pollens, LEA proteins have been found to protect against desiccation, cold, or high salinity in a variety of organisms, including the bacterium Deinococcus radiodurans, nematode Caenorhabditis elegans, Artemia, and rotifers.

<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>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.

Adineta ricciae is a species of freshwater rotifers in the family Adinetidae. It was first described in 2005 after being discovered by chance in dry mud beside a billabong in Australia. It is used as a model organism as it is easy to keep in culture.

John Henry Crowe is an American comparative physiologist. He is primarily known for his work on the mechanisms dehydration and rehydration of cryptobiotic organism, including tardigrades. His work included the discovery of trehalose as a cryoprotectant for cell membranes and the use of trahalose and other cryoprotectants for the preservation of human blood components including platelets for longer-term storage

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.

Panagrolaimus superbus is a species of terrestrial free-living nematode (roundworm). P. superbus, like other species within the Panagrolaimus genus, exhibits the ability to enter anhydrobiosis for extended periods of time.

<i>Panagrolaimus kolymaensis</i> Species of nematode

Panagrolaimus kolymaensis is a species of nematode.

References

  1. Bartels, Dorothea; Salamini, Francesco (December 2001). "Desiccation Tolerance in the Resurrection Plant Craterostigma plantagineum. A Contribution to the Study of Drought Tolerance at the Molecular Level". Plant Physiology. 127 (4): 1346–1353. doi:10.1104/pp.010765. PMC   1540161 . PMID   11743072.
  2. Calahan, Dean; Dunham, Maitreya; DeSevo, Chris; Koshland, Douglas E (October 2011). "Genetic analysis of desiccation tolerance in Sachharomyces cerevisiae". Genetics. 189 (2): 507–519. doi:10.1534/genetics.111.130369. PMC   3189811 . PMID   21840858.
  3. Shen-Miller, J; Mudgett, Mary Beth; Schopf, J William; Clarke, Steven; Berger, Rainer (November 1995). "Exceptional seed longevity and robust growth: Ancient sacred lotus from China". American Journal of Botany. 82 (11): 1367–1380. doi:10.2307/2445863. JSTOR   2445863.
  4. Erkut, Cihan; Penkov, Sider; Fahmy, Karim; Kurzchalia, Teymuras V (January 2012). "How worms survive desiccation: Trehalose pro water". Worm. 1 (1): 61–65. doi:10.4161/worm.19040. PMC   3670174 . PMID   24058825.
  5. Tunnacliffe, Alan; Lapinski, Jens; McGee, Brian (September 2005). "A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers". Hydrobiologia. 546 (1): 315–321. doi:10.1007/s10750-005-4239-6. S2CID   13072689.
  6. Erkut, Cihan; Penkov, Sider; Khesbak, Hassan; Vorkel, Daniela; Verbavatz, Jean-Marc; Fahmy, Karim; Kurzchalia, Teymuras V (August 2011). "Trehalose renders the dauer larva of Caenorhabditis elegans resistant to extreme desiccation". Current Biology. 21 (15): 1331–1336. doi: 10.1016/j.cub.2011.06.064 . PMID   21782434. S2CID   18145344.
  7. Erkut, Cihan; Vasilj, Andrej; Boland, Sebastian; Habermann, Bianca; Shevchenko, Andrej; Kurzchalia, Teymuras V (December 2013). "Molecular strategies of the Caenorhabditis elegans dauer larva to survive extreme desiccation". PLOS ONE. 8 (12): e82473. Bibcode:2013PLoSO...882473E. doi: 10.1371/journal.pone.0082473 . PMC   3853187 . PMID   24324795.
  8. "High hopes for fridge-free jabs". BBC News. 2004-10-19.
  9. Yang, Geer; Gilstrap, Kyle; Zhang, Aili; Xu, Lisa X.; He, Xiaoming (1 June 2010). "Collapse temperature of solutions important for lyopreservation of living cells at ambient temperature". Biotechnology and Bioengineering. 106 (2): 247–259. doi:10.1002/bit.22690. PMID   20148402. S2CID   20748794.
  10. Chakraborty, Nilay; Chang, Anthony; Elmoazzen, Heidi; Menze, Michael A.; Hand, Steven C.; Toner, Mehmet (2011). "A Spin-Drying Technique for Lyopreservation of Mammalian Cells". Annals of Biomedical Engineering. 39 (5): 1582–1591. doi:10.1007/s10439-011-0253-1. PMID   21293974. S2CID   11204697.
  11. Yang G, Gilstrap K, Zhang A, Xu LX, He X. "Collapse temperature of solutions important for lyopreservation of living cells at ambient temperatures." Biotechnol Bioeng. 2010 Jun 1;106(2):247–259.
  12. Chakraborty N, Chang A, Elmoazzen H, Menze MA, Hand SC, Toner M. "A spin-drying technique for lyopreservation of mammalian cells". Ann Biomed Eng. 2011 May;39(5):1582–1591.
  13. Clegg et al. 1999
  14. Marcus et al., 1994
  15. Crowe and Cooper, 1971
  16. Reiswig and Miller, 1998
  17. Clegg, James S. (2001). "Cryptobiosis – a peculiar state of biological organization". Comparative Biochemistry and Physiology B. 128 (4): 613–624. doi:10.1016/S1096-4959(01)00300-1. PMID   11290443. Closed Access logo transparent.svg
  18. 1 2 Møbjerg, N.; Halberg, K. A.; Jørgensen, A.; Persson, D.; Bjørn, M.; Ramløv, H.; Kristensen, R. M. (2011). "Survival in extreme environments – on the current knowledge of adaptations in tardigrades". Acta Physiologica. 202 (3): 409–420. doi:10.1111/j.1748-1716.2011.02252.x. PMID   21251237. S2CID   20894284.
  19. "Frozen Lobsters Brought Back to Life". 18 March 2004.
  20. C. Michael Hogan (2008) Makgadikgadi, The Megalithic Portal, ed. A. Burnham
  21. Piper, Ross (2007), Extraordinary Animals: An Encyclopedia of Curious and Unusual Animals, Greenwood Press.
  22. Illinois Wesleyan University Tardigrade Facts
  23. Watanabe, Masahiko (2006). "Anhydrobiosis in invertebrates". Appl. Entomol. Zool. 41 (1): 15–31. doi: 10.1303/aez.2006.15 .

Further reading