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New insights into the limited thermotolerance of anhydrobiotic tardigrades.

ABSTRACT: The recent discovery of an upper limit in the tolerance of an extremotolerant tardigrade to high temperatures is astounding. Although these microinvertebrates are able to endure severe environmental conditions, including desiccation, freezing and high levels of radiation, high temperatures seem to be an Achilles' heel for active tardigrades. Moreover, exposure-time appears to be a limiting factor for the heat stress tolerance of the otherwise highly resilient desiccated (anhydrobiotic) tardigrades. Indeed, the survival rate of desiccated tardigrades exposed to high temperatures for 24 hours is significantly lower than for exposures of only 1 hour. Here, we investigate the effect of 1 week of high temperature exposures on desiccated tardigrades with the aim of elucidating whether exposure-times longer than 24 hours decrease survival even further. From our analyses we estimate a significant decrease in the 50% mortality temperature from 63ºC to 56ºC for Ramazzottius varieornatus exposed to high temperatures in the desiccated tun state for 24 hours and 1 week, respectively. This negative correlation between exposure-time and tolerance to high temperatures probably results from the interference of intracellular temperature with the homeostasis of macromolecules. We hypothesize that high temperatures denature molecules that play a vital role in sustaining and protecting the anhydrobiotic state.

SUBMITTER: Neves RC

PROVIDER: S-EPMC7518453 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundTardigrades are small, multicellular invertebrates which are able to survive times of unfavourable environmental conditions using their well-known capability to undergo cryptobiosis at any stage of their life cycle. Milnesium tardigradum has become a powerful model system for the analysis of cryptobiosis. While some genetic information is already available for Milnesium tardigradum the proteome is still to be discovered.Principal findingsHere we present to the best of our knowledge the first comprehensive study of Milnesium tardigradum on the protein level. To establish a proteome reference map we developed optimized protocols for protein extraction from tardigrades in the active state and for separation of proteins by high resolution two-dimensional gel electrophoresis. Since only limited sequence information of M. tardigradum on the genome and gene expression level is available to date in public databases we initiated in parallel a tardigrade EST sequencing project to allow for protein identification by electrospray ionization tandem mass spectrometry. 271 out of 606 analyzed protein spots could be identified by searching against the publicly available NCBInr database as well as our newly established tardigrade protein database corresponding to 144 unique proteins. Another 150 spots could be identified in the tardigrade clustered EST database corresponding to 36 unique contigs and ESTs. Proteins with annotated function were further categorized in more detail by their molecular function, biological process and cellular component. For the proteins of unknown function more information could be obtained by performing a protein domain annotation analysis. Our results include proteins like protein member of different heat shock protein families and LEA group 3, which might play important roles in surviving extreme conditions.ConclusionsThe proteome reference map of Milnesium tardigradum provides the basis for further studies in order to identify and characterize the biochemical mechanisms of tolerance to extreme desiccation. The optimized proteomics workflow will enable application of sensitive quantification techniques to detect differences in protein expression, which are characteristic of the active and anhydrobiotic states of tardigrades.

Project description:The open space is a hostile environment for all lifeforms not only due to vacuum, high radiation, low atmospheric pressure, and extremely low temperature, but also the absence of the geomagnetic field. The geomagnetic field protects Earth mainly from corpuscular radiation, that is, solar wind and cosmic radiation, but above all it influences organisms, including their cells, tissues and organs. Moreover, numerous studies conducted on plants and animals confirmed that hypomagnetic conditions (the term referring to all situations when the magnetic field is weaker than the typical geomagnetic field) have significant influence on the metabolism of living organisms. Although many studies dealt with a variety of aspects related mainly to the influence of hypomagnetic conditions on human health. Very few studies have considered the influence of hypomagnetic conditions on extremophiles. Astrobiologists have long been testing different extremofiles to find out if any multicellular organisms are able to survive in extreme conditions of open space. Among all multicellular extremophiles fit for such research, water bears (Tardigrada) are the most interesting. Not only are they one of the most resistant organisms on Earth, but results obtained from studies on these invertebrates can be extrapolated or applied to vertebrates (including humans). Despite this, studies on the influence of hypomagnetic conditions on tardigrades are rare, so far. In the present study, to test the influence of hypomagnetic conditions on the process of anhydrobiosis while entering and returning from anhydrobiosis, we used two terrestrial anhydrobiotic species that are Echiniscus testudo and Milnesium inceptum. To exclude the ambient magnetic field, experiments were carried out in a special magnetic field shielding chamber. In total, three experiments were conducted: (a) tardigrades in anhydrobiosis, (b) tardigrades entering anhydrobiosis and (c) tardigrades returning to active life. The obtained results clearly showed that even partial isolation from the geomagnetic field, that is, hypomagnetic conditions, has negative influence on anhydrobiotic abilities of both tested tardigrade species. In both species we observed lower survivability rate while entering anhydrobiosis, in anhydrobiotic state and returning to the active state. What is more, we observed a higher mortality rate in Ech. testudo than Mil. inceptum which suggest that different species response to the hypomagnetic conditions in different way. In conclusion, while current knowledge on the influence of hypomagnetic conditions on mortality of invertebrates is very limited, our results suggest that the presence of the magnetic field is a very important factor which should be considered in further research focused on potential survival of Earth organisms in outer space, spacecrafts or different planets and moons.

Project description:BackgroundAlthough molecular analyses have contributed to a better resolution of the animal tree of life, the phylogenetic position of tardigrades (water bears) is still controversial, as they have been united alternatively with nematodes, arthropods, onychophorans (velvet worms), or onychophorans plus arthropods. Depending on the hypothesis favoured, segmental ganglia in tardigrades and arthropods might either have evolved independently, or they might well be homologous, suggesting that they were either lost in onychophorans or are a synapomorphy of tardigrades and arthropods. To evaluate these alternatives, we analysed the organisation of the nervous system in three tardigrade species using antisera directed against tyrosinated and acetylated tubulin, the amine transmitter serotonin, and the invertebrate neuropeptides FMRFamide, allatostatin and perisulfakinin. In addition, we performed retrograde staining of nerves in the onychophoran Euperipatoides rowelli in order to compare the serial locations of motor neurons within the nervous system relative to the appendages they serve in arthropods, tardigrades and onychophorans.ResultsContrary to a previous report from a Macrobiotus species, our immunocytochemical and electron microscopic data revealed contralateral fibres and bundles of neurites in each trunk ganglion of three tardigrade species, including Macrobiotus cf. harmsworthi, Paramacrobiotus richtersi and Hypsibius dujardini. Moreover, we identified additional, extra-ganglionic commissures in the interpedal regions bridging the paired longitudinal connectives. Within the ganglia we found serially repeated sets of serotonin- and RFamid-like immunoreactive neurons. Furthermore, our data show that the trunk ganglia of tardigrades, which include the somata of motor neurons, are shifted anteriorly with respect to each corresponding leg pair, whereas no such shift is evident in the arrangement of motor neurons in the onychophoran nerve cords.ConclusionsTaken together, these data reveal three major correspondences between the segmental ganglia of tardigrades and arthropods, including (i) contralateral projections and commissures in each ganglion, (ii) segmentally repeated sets of immunoreactive neurons, and (iii) an anteriorly shifted (parasegmental) position of ganglia. These correspondences support the homology of segmental ganglia in tardigrades and arthropods, suggesting that these structures were either lost in Onychophora or, alternatively, evolved in the tardigrade/arthropod lineage.

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New insights into the limited thermotolerance of anhydrobiotic tardigrades.

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