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Differential mechanisms of tolerance to extreme environmental conditions in tardigrades.

ABSTRACT: Tardigrades, also known as water bears, are small aquatic animals that inhabit marine, fresh water or limno-terrestrial environments. While all tardigrades require surrounding water to grow and reproduce, species living in limno-terrestrial environments (e.g. Ramazzottius varieornatus) are able to undergo almost complete dehydration by entering an arrested state known as anhydrobiosis, which allows them to tolerate ionic radiation, extreme temperatures and intense pressure. Previous studies based on comparison of the genomes of R. varieornatus and Hypsibius dujardini - a less tolerant tardigrade - have pointed to potential mechanisms that may partially contribute to their remarkable ability to resist extreme physical conditions. In this work, we have further annotated the genomes of both tardigrades using a guided approach in search for novel mechanisms underlying the extremotolerance of R. varieornatus. We have found specific amplifications of several genes, including MRE11 and XPC, and numerous missense variants exclusive of R. varieornatus in CHEK1, POLK, UNG and TERT, all of them involved in important pathways for DNA repair and telomere maintenance. Taken collectively, these results point to genomic features that may contribute to the enhanced ability to resist extreme environmental conditions shown by R. varieornatus.

SUBMITTER: Carrero D

PROVIDER: S-EPMC6797769 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Differential mechanisms of tolerance to extreme environmental conditions in tardigrades.

Carrero Dido D Pérez-Silva José G JG Quesada Víctor V López-Otín Carlos C

Scientific reports 20191017 1

Tardigrades, also known as water bears, are small aquatic animals that inhabit marine, fresh water or limno-terrestrial environments. While all tardigrades require surrounding water to grow and reproduce, species living in limno-terrestrial environments (e.g. Ramazzottius varieornatus) are able to undergo almost complete dehydration by entering an arrested state known as anhydrobiosis, which allows them to tolerate ionic radiation, extreme temperatures and intense pressure. Previous studies base ...[more]

PMID: 31624306

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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:Tardigrades are microscopic aquatic animals renowned for their tolerance toward extreme environmental conditions. The current study is the first to investigate their tolerance toward heavy metals and we present a novel tardigrade toxicant tolerance assay based on activity assessments as a measure of survival. Specifically, we compare tolerance toward copper in four species representing different evolutionary lineages, habitats and adaptation strategies, i.e., a marine heterotardigrade, Echiniscoides sigismundi, a limno-terrestrial heterotardigrade, Echiniscus testudo, a limno-terrestrial eutardigrade, Ramazzottius oberhaeuseri, and a marine eutardigrade, Halobiotus crispae. The latter was sampled at a time of year, when the population is predominantly represented by aberrant P1 cysts, while the other species were in normal active states prior to exposure. Based on volume measurements and a general relation between body mass and copper tolerance, expected tardigrade EC50 values were estimated at 0.5-2 μg l-1. Following 24 h of exposure, tolerance was high with no apparent link to lineage or habitat. EC50s (95% CI), 24 h after exposure, were estimated at 178 (168-186) and 310 (295-328) μg l-1, respectively, for E. sigismundi and R. oberhaeuseri, whereas E. testudo and H. crispae were less affected. Highest tolerance was observed in H. crispae with a mean ± s.e.m. activity of 77 ± 2% (n = 3) 24 h after removal from ~3 mg l-1 copper, suggesting that tardigrade cysts have increased tolerance toward toxicants. In order to identify putative tolerance related genes, an E. sigismundi transcriptome was searched for key enzymes involved in osmoregulation, antioxidant defense and copper metabolism. We found high expression of Na/K ATPase and carbonic anhydrase, known targets for copper. Our transcriptome, furthermore, revealed high expression of antioxidant enzymes, copper transporters, ATOX1, and a Cu-ATPase. In summary, our results indicate that tardigrades express well-known key osmoregulatory enzymes, supporting the hypothesis that copper inhibits sodium turnover as demonstrated for other aquatic organisms. Tardigrades, nevertheless, have high tolerance toward the toxicant, which is likely linked to high expression of antioxidant enzymes and an ability to enter dormant states. Tardigrades, furthermore, seem to have a well-developed battery of cuproproteins involved in copper homeostasis, providing basis for active copper sequestering and excretion.

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Project description:Environmental conditions unsuitable for microbial growth are the rule rather than the exception in most habitats. In response to this, microorganisms have developed various strategies to withstand environmental conditions that limit active growth. Endospore-forming Firmicutes (EFF) deploy a myriad of survival strategies in order to resist adverse conditions. Like many bacterial groups, they can form biofilms and detect nutrient scarcity through chemotaxis. Moreover, within this paraphyletic group of Firmicutes, ecophysiological optima are diverse. Nonetheless, a response to adversity that delimits this group is the formation of wet-heat resistant spores. These strategies are energetically demanding and therefore might affect the biological success of EFF. Therefore, we hypothesize that abundance and diversity of EFF should be maximized in those environments in which the benefits of these survival strategies offsets the energetic cost. In order to address this hypothesis, geothermal and mineral springs and drillings were selected because in these environments of steep physicochemical gradients, diversified survival strategies may become a successful strategy.We collected 71 samples from geothermal and mineral environments characterized by none (null), single or multiple limiting environmental factors (temperature, pH, UV radiation, and specific mineral composition). To measure success, we quantified EFF gene copy numbers (GCN; spo0A gene) in relation to total bacterial GCN (16S rRNA gene), as well as the contribution of EFF to community composition. The quantification showed that relative GCN for EFF reached up to 20% at sites characterized by multiple limiting environmental factors, whereas it corresponded to less than 1% at sites with one or no limiting environmental factor. Pyrosequencing of the 16S rRNA gene supports a higher contribution of EFF at sites with multiple limiting factors. Community composition suggested a combination of phylotypes for which active growth could be expected, and phylotypes that are most likely in the state of endospores, in all the sites. In summary, our results suggest that diversified survival strategies, including sporulation and metabolic adaptations, explain the biological success of EFF in geothermal and natural springs, and that multiple extreme environmental factors favor the prevalence of EFF.

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Differential mechanisms of tolerance to extreme environmental conditions in tardigrades.

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Differential mechanisms of tolerance to extreme environmental conditions in tardigrades.

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