Back to the roots, desiccation and radiation resistances are ancestral characters in bdelloid rotifers

Abstract

Background Bdelloid rotifers are micro-invertebrates distributed worldwide, from temperate latitudes to the most extreme areas of the planet like Antarctica or the Atacama Desert. They have colonized any habitat where liquid water is temporarily available, including terrestrial environments such as soils, mosses, and lichens, tolerating desiccation and other types of stress such as high doses of ionizing radiation (IR). It was hypothesized that bdelloid desiccation and radiation resistance may be attributed to their potential ability to repair DNA double-strand breaks (DSBs). Here, these properties are investigated and compared among nine bdelloid species collected from both mild and harsh habitats, addressing the correlation between the ability of bdelloid rotifers to survive desiccation and their capacity to repair massive DNA breakage in a phylogenetically explicit context. Our research includes both specimens isolated from habitats that experience frequent desiccation (at least 1 time per generation), and individuals sampled from habitats that rarely or never experienced desiccation. Results Our analysis reveals that DNA repair prevails in somatic cells of both desiccation-tolerant and desiccation-sensitive bdelloid species after exposure to X-ray radiation. Species belonging to both categories are able to withstand high doses of ionizing radiation, up to 1000 Gy, without experiencing any negative effects on their survival. However, the fertility of two desiccation-sensitive species, Rotaria macrura and Rotaria rotatoria, was more severely impacted by low doses of radiation than that of desiccation-resistant species. Surprisingly, the radioresistance of desiccation-resistant species is not related to features of their original habitat. Indeed, bdelloids isolated from Atacama Desert or Antarctica were not characterized by a higher radioresistance than species found in more temperate environments. Conclusions Tolerance to desiccation and radiation are supported as ancestral features of bdelloid rotifers, with a group of species of the genus Rotaria having lost this trait after colonizing permanent water habitats. Together, our results provide a comprehensive overview of the evolution of desiccation and radiation resistance among bdelloid rotifers.

Long-Term Survivability of Tardigrade Paramacrobiotus experimentalis (Eutardigrada) at Increased Magnesium Perchlorate Levels: Implications for Astrobiological Research

“…In general, perchlorates are well known to be toxic to vertebrates and invertebrates, e.g., Caenorhabditis elegans (Maupas, 1900) at levels as low as 0.00005% [ 18 ] or to Daphnia magna (Straus, 1820) at 0.05% [ 19 ]. However, selected invertebrates are known for their resistance to various extreme conditions [ 20 , 21 ]. Among them, tardigrades, free-living microinvertebrates associated with terrestrial and aquatic environments, stand out to the point where they have gained the popular title of the “toughest animals on Earth” [ 22 , 23 ].…”

Tracing the serendipitous genesis of radiation resistance

“…strain PCC 7120, Deinococcus deserti, etc. ( de Groot et al, 2009;Hespeels et al, 2023;Singh et al, 2013). Similarly, direct damage causes protein inactivation or damage to membrane lipids or structural polysaccharides may impair membrane integrity, at higher doses of gamma rays (Reisz et al, 2014).…”

Weak effect of urbanization on bdelloid rotifers living in lichens

“…Some species of bdelloid rotifers, and other microscopic animals, exhibit large distribution ranges across the world, potentially owing to their highly resistant dormant stages that allow long-range passive dispersal even between continents [ 14 ]. Yet, even if some bdelloid rotifer species may have wide distributions, different species are known to be adapted to different environmental conditions [ 15 , 16 ] as also observed in monogonont rotifers [ 17 ]. We can thus reliably assume that anthropogenic effects could lead to detectable species decline and/or loss for bdelloid rotifers.…”

“…Generally, bdelloid rotifers thrive in any habitat where water becomes available, even for short periods, owing to their peculiar ability to survive complete desiccation at any life cycle stage. Some rotifer species also occur in so-called extreme habitats, both of natural origin, such as the Atacama desert [ 16 ], high mountains [ 18 ], the inhospitable polar regions [ 19 ] and of anthropogenic origin, such as mine lakes [ 20 ] and heavy metal polluted waters [ 21 ]. However, the few species that can indeed occur in anthropogenically modified environments are those that naturally occur in similar habitats, for example, with comparable levels of low pH or high load of heavy metals [ 22 , 23 ].…”