A Comparative Ultrastructure Study of the Tardigrade Ramazzottius varieornatus In The Hydrated State, After Desiccation and During the Process of Rehydration
Tardigrades can survive hostile environments such as desiccation by adopting a state of anhydrobiosis. Numerous tardigrade species have been described thus far, and recent genome and transcriptome analyses revealed that several distinct strategies were employed to cope with harsh environments depending on the evolutionary lineages.
Detailed analyses at the cellular and subcellular levels are essential to complete these data. In this work, we analyzed a tardigrade species that can withstand rapid dehydration, Ramazzottius varieornatus. Surprisingly, we noted an absence of the anhydrobiotic-specific extracellular structure previously described for the Hypsibius exemplaris species. Both Ramazzottius varieornatus and Hypsibius exemplaris belong to the same evolutionary class of Eutardigrada. Nevertheless, our observations reveal discrepancies in the anhydrobiotic structures correlated with the variation in the anhydrobiotic mechanisms.
A comparative ultrastructure study of the tardigrade Ramazzottius varieornatus in the hydrated state, after desiccation and during the process of rehydration — PLoS
Introduction
Tardigrades are tiny metazoan animals that range in size from approximately 0.1–1.2 mm and have four pairs of legs [1]. They can be called “water bears” because of their appearance and “moss piglets” because of where they can be found. Nearly 1500 tardigrades species have thus far been described [2], which are distributed from the depths of the oceans to the highest mountain peaks [3]. The worldwide distribution of tardigrade species can be either endemic or cosmopolitan [4–8], and their transport by birds or snails has recently been suggested [9–11].
As earlier as their discovery in the 18th century [12], tardigrades have demonstrated an ability to adopt a latent state due to a shortage of water, which is called anhydrobiosis. These tardigrades, rather terrestrial species, can enter an anhydrobiosis state in response to desiccation to form an anhydrobiote, allowing the organism to wait for the return of water [13, 14].
Thus, by reaching nearly complete desiccation, tardigrades can survive for many years as anhydrobiotes [15–18]. During the course of desiccation, tardigrades contract and retract their whole body to assume a characteristic “tun”-shaped anhydrobiote structure. Tardigrades can then lose up to 97% of their bound and free body water content [19].
Graphical representation of the ultrastructural divergences between Ram. varieornatus and Hys. exemplaris during the dehydration and anhydrobiote formation processes. Abstract design: Laurence Meslin CNRS, ISEM 2023. https://doi.org/10.1371/journal.pone.0302552.g006 — PLoS
Other invertebrates, such as rotifers, nematodes and dipteran larvae [12, 20–23], can enter anhydrobiosis and some of them are also tolerant to other extreme physical stresses. For example, the nematode Panagrolaimus superbus displays tolerance to ultra-low temperature (-196°C), X-radiations (500Gy) or ultracentrifugation (400,000xg) [24] and bdelloids rotifers are able to withstand high doses of ionizing radiation, up to 1000 Gy [25, 26].
Likewise, Adineta vaga is known for its resistance to X-ray, protons and Fe ions [27]. However the particularity of the tardigrade is that it resists a more extensive set of stresses. Indeed, tardigrades are resistant to temperatures ranging from -272 to +150°C [28, 29], very high pressures (up to 7.5 Gpa) equivalent to that at a depth of up to 180 km from the Earth’s surface [30], radiation at levels up to 5000 Gy [31–33] and exposure to solar radiation at a low Earth orbit in a space vacuum during a ten-day space flight [34]. These characteristics make them an emerging model for space biology [35].
To date, the genomes of four tardigrade species are available [36]. The genomes of two Eutardigrada species: Ramazzottius varieornatus (Ram. varieornatus) and Hypsibius exemplaris (Hys. exemplaris) [37–39], enabled the identification of gene products involved in anhydrobiosis. For instance, the Dsup (damage suppressor) gene was identified in Ram.
Varieornatus and was suggested to protect both human and plant cells from gamma ray irradiation [31, 38, 40] as well as human cultured cells from oxidation by free radicals [31, 38]. The molecular capacity of the Dsup gene products to protect nucleosomes from direct oxidation by hydroxyl radicals was thereafter evidenced by an in vitro assay [41].
While Ram. varieornatus is tolerant to a rapid desiccation process (minutes), Hys. exemplaris can undergo effective anhydrobiosis after only an obligate preconditioning period (hours) [14, 36, 42].
A comparative ultrastructure study of the tardigrade Ramazzottius varieornatus in the hydrated state, after desiccation and during the process of rehydration, PLoS (open access)
Astrobiology
