Tardigrade specific proteins

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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.

Contents

History

The mechanisms of tardigrade desiccation protection were originally thought to result from high levels of the sugar trehalose. Trehalose is used by organisms like yeast to avoid desiccation in dry environments by working with heat shock proteins [1] to keep desiccation-sensitive proteins in solution. [2] [3] However, while tardigrades can accumulate small levels of trehalose, the levels are insufficient to provide protection from extreme conditions. [4] Other molecules which help certain organisms avoid cellular desiccation include late embryogenesis abundant proteins, which provide protection to embryonic cotton seeds. [5] Certain proteins actually responsible for the tardigrade's hardiness, including the cytoplasmic and secreted abundant heat soluble proteins, were discovered when searching for late embryogenesis abundant proteins in tardigrades. [6]

One strategy used by the tardigrade to survive in dry environments is anhydrobiosis. Anhydrobiosis is a process in which an organism can lose nearly all of its water and enter an ametabolic state. [7]

Function

Tardigrade specific proteins are a type of intrinsically disordered proteins, which have no predetermined shape or task. These proteins use many different conformations, called an ensemble, to move through different structures. Because of this, intrinsically disordered proteins may react strongly to the environment they inhabit. [8] There are three families of tardigrade specific proteins, each named after where the protein is localized within a cell. These proteins are similar to late embryogenesis abundant proteins but are specific to tardigrades. The three families do not resemble each other and are expressed or enriched during desiccation. Unlike traditional proteins, intrinsically disordered proteins do not precipitate out of solution or denature during high heat. [9] Tardigrades rely on these proteins to help them survive extreme environments, where they put their bodies in a dehydrated state called a tun. In most organisms, dehydration causes problems for cells, which need a hydrated environment for their proteins to function. However, tardigrade specific proteins assist in preventing aggregation of cell contents upon dehydration, and maintain the integrity of the cell membrane upon rehydration.

Types

Cytoplasmic

Cytoplasmic abundant heat soluble (CAHS) proteins are highly expressed in response to desiccation. There are two hypotheses for their function in tardigrades. The vitrification hypothesis is the idea that, when a tardigrade becomes desiccated, the viscosity within its cells increases to the point that denaturation and membrane fusion in proteins would stop. [10] A second hypothesis, the water replacement hypothesis, posits that CAHS proteins replace water in other desiccation-sensitive proteins, protecting the hydrogen bonds normally reliant on water. [11] CAHS proteins are dispersed throughout the cell in normal conditions, but form a network of filaments during environmentally stressful conditions. This network transforms the cytoplasm into a gel-like matrix and prevents the cell from collapsing as water leaches out. [12] This state is reversible and the proteins disaggregate when exposed to less stressful conditions. [13]

When forming the filament network, CAHS proteins have long helical domains that interact in a coiled manner with each other. These interactions are possible due to the proteins' partial disorder, with two flexible tails surrounding the helical domains. [14]

CAHS proteins have been studied to observe their interactions with trehalose, a sugar used by other species to prevent desiccation. Trehalose was found to interact at higher levels with CAHS proteins than other sugars such as sucrose. [15] Trehalose averages only 1% in most species of tardigrades, and in no species more than 3%, indicating that tardigrades use other strategies to tolerate dehydration. [6]

Tardigrade CAHS protein injected into mice produced no inflammatory response or hemolysis. [16]

Secreted

Secreted abundant heat soluble (SAHS) proteins are similar to fatty acid-binding proteins, notably in their structure with an antiparallel beta-barrel and internal fatty acid binding pocket. [17] [18] SAHS proteins are often secreted into media and associated with special extracellular structures. [19] Dried tardigrades have an abundance of secretory cells which are not found in hydrated individuals. The mechanism behind SAHS proteins has not yet been determined, but the presence of secretory cells only during desiccation suggests they are used to protect cells during periods of dehydration.

Mitochondrial

Mitochondrial abundant heat soluble (MAHS) proteins are localized in mitochondria and are responsible for protecting mitochondria during desiccation. [20] Because of its role in metabolizing reactive oxygen species, the mitochondrion is an important organelle to protect in extreme environments. During dehydration, the mitochondria of tardigrades grow much smaller and lose their cristae. [5] MAHS proteins may act to replace water in the membrane of the mitochondria, preventing uneven rehydration and membrane rupture. [21] Mitochondria and muscle contraction due to mitochondria are essential for tardigrade to enter the "tun" state of anhydrobiosis. [22]

Dsup (damage suppressor protein)

Dsup is a DNA-associating protein, unique to the tardigrade, [23] that suppresses the occurrence of DNA breaks by radiation. [24] [25] [26] [27] Dsup localized to nuclear DNA reduces single-strand breaks and double-strand breaks when subjected to ionizing radiation. [28]

LEA Proteins

Late embryogenesis abundant proteins (LEA proteins) are proteins that protect against protein aggregation due to dehydration or osmotic stress. However, no LEA proteins have been found in tardigrades. [6]

Related Research Articles

<span class="mw-page-title-main">Cytosol</span> Liquid found in cells

The cytosol, also known as cytoplasmic matrix or groundplasm, is one of the liquids found inside cells. It is separated into compartments by membranes. For example, the mitochondrial matrix separates the mitochondrion into many compartments.

<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. The word desiccation comes from Latin de- 'thoroughly' and siccare 'to dry'.

<span class="mw-page-title-main">Alpha-synuclein</span> Protein found in humans

Alpha-synuclein (aSyn) is a protein that, in humans, is encoded by the SNCA gene. Alpha-synuclein is a neuronal protein that regulates synaptic vesicle trafficking and subsequent neurotransmitter release.

<span class="mw-page-title-main">Lipoid congenital adrenal hyperplasia</span> Medical condition

Lipoid congenital adrenal hyperplasia is an endocrine disorder that is an uncommon and potentially lethal form of congenital adrenal hyperplasia (CAH). It arises from defects in the earliest stages of steroid hormone synthesis: the transport of cholesterol into the mitochondria and the conversion of cholesterol to pregnenolone—the first step in the synthesis of all steroid hormones. Lipoid CAH causes mineralocorticoid deficiency in affected infants and children. Male infants are severely undervirilized causing their external genitalia to look feminine. The adrenals are large and filled with lipid globules derived from cholesterol.

<span class="mw-page-title-main">GroEL</span> Protein-coding gene in the species Homo sapiens

GroEL is a protein which belongs to the chaperonin family of molecular chaperones, and is found in many bacteria. It is required for the proper folding of many proteins. To function properly, GroEL requires the lid-like cochaperonin protein complex GroES. In eukaryotes the organellar proteins Hsp60 and Hsp10 are structurally and functionally nearly identical to GroEL and GroES, respectively, due to their endosymbiotic origin.

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">Intrinsically disordered proteins</span> Protein without a fixed 3D structure

In molecular biology, an intrinsically disordered protein (IDP) is a protein that lacks a fixed or ordered three-dimensional structure, typically in the absence of its macromolecular interaction partners, such as other proteins or RNA. IDPs range from fully unstructured to partially structured and include random coil, molten globule-like aggregates, or flexible linkers in large multi-domain proteins. They are sometimes considered as a separate class of proteins along with globular, fibrous and membrane proteins.

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.

Dehydrin (DHN) is a multi-family of proteins present in plants that is produced in response to cold and drought stress. DHNs are hydrophilic, reliably thermostable, and disordered. They are stress proteins with a high number of charged amino acids that belong to the Group II Late Embryogenesis Abundant (LEA) family. DHNs are primarily found in the cytoplasm and nucleus but more recently, they have been found in other organelles, like mitochondria and chloroplasts.

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>Ramazzottius</i> Genus of tardigrades

Ramazzottius is a genus of water bear or moss piglet, a tardigrade in the class Eutardigrada.

<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</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.

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

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.

References

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  2. ↑ Tapia H, Young L, Fox D, Bertozzi CR, Koshland D (May 2015). "Increasing intracellular trehalose is sufficient to confer desiccation tolerance to Saccharomyces cerevisiae". Proceedings of the National Academy of Sciences of the United States of America. 112 (19): 6122–6127. Bibcode:2015PNAS..112.6122T. doi: 10.1073/pnas.1506415112 . PMC   4434740 . PMID   25918381.
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  28. ↑ Aguilar R, Hickman AR, Tyler JK (2023). "Multivalent binding of the tardigrade Dsup protein to chromatin promotes yeast survival and longevity upon exposure to oxidative damage". Research Square : rs.3.rs–3182883. doi:10.21203/rs.3.rs-3182883/v1. PMC   10402244 . PMID   37546815.
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