Tolerance to Gamma Radiation in the Tardigrade Hypsibius dujardini from Embryo to Adult Correlate Inversely with Cellular Proliferation

Abstract

Tardigrades are highly tolerant to desiccation and ionizing radiation but the mechanisms of this tolerance are not well understood. In this paper, we report studies on dose responses of adults and eggs of the tardigrade Hypsibius dujardini exposed to gamma radiation. In adults the LD50/48h for survival was estimated at ~ 4200 Gy, and doses higher than 100 Gy reduced both fertility and hatchability of laid eggs drastically. We also evaluated the effect of radiation (doses 50 Gy, 200 Gy, 500 Gy) on eggs in the early and late embryonic stage of development, and observed a reduced hatchability in the early stage, while no effect was found in the late stage of development. Survival of juveniles from irradiated eggs was highly affected by a 500 Gy dose, both in the early and the late stage. Juveniles hatched from eggs irradiated at 50 Gy and 200 Gy developed into adults and produced offspring, but their fertility was reduced compared to the controls. Finally we measured the effect of low temperature during irradiation at 4000 Gy and 4500 Gy on survival in adult tardigrades, and observed a slight delay in the expressed mortality when tardigrades were irradiated on ice. Since H. dujardini is a freshwater tardigrade with lower tolerance to desiccation compared to limno-terrestrial tardigrades, the high radiation tolerance in adults, similar to limno-terrestrial tardigrades, is unexpected and seems to challenge the idea that desiccation and radiation tolerance rely on the same molecular mechanisms. We suggest that the higher radiation tolerance in adults and late stage embryos of H. dujardini (and in other studied tardigrades) compared to early stage embryos may partly be due to limited mitotic activity, since tardigrades have a low degree of somatic cell division (eutely), and dividing cells are known to be more sensitive to radiation.

Tolerance to Gamma Radiation in the Marine Heterotardigrade, Echiniscoides sigismundi

“…High radiation tolerance therefore is not restricted to the class Eutardigrada but seems to have a wide taxonomic distribution within the phylum Tardigrada. However, in contrast to previous dose-response studies with gamma rays in eutardigrades, which exhibit LD50 values in the range of 3–5 kGy, 1–2 days after irradiation [5,6,7], calculated LD50 values of E . sigismundi were considerably lower.…”

“…sigismundi were considerably lower. Already at 1 kGy the effect of irradiation on animal activity was considerable, while in the eutardigrades Macrobiotus areolatus [4], Richtersius coronifer [5], Milnesium tardigradum [6], and Hypsibius dujardini [7], doses of 3 kGy or higher were required to significantly reduce viability. Thus, under the current protocol, E .…”

“…They also belong to the most radiation tolerant animals on Earth and several studies have documented a very high tolerance of adult tardigrades to both low-LET (Linear Energy Transfer) radiation (X-rays: [4]; gamma rays: [5,6,7]), high-LET radiation (alpha particles: [6]; protons: [8]), and UV radiation [9,10]. Tardigrades are also the only animals so far that have survived the combined exposure to cosmic radiation, UV radiation and vacuum under real space conditions [11].…”

“…It is also clear that the tolerance is not restricted to the desiccated anhydrobiotic state in tardigrades, but is expressed also in active hydrated animals. Embryos are considerably more sensitive to radiation, particularly in the early stage of development [7,13,14,15]. …”

“…The majority of previous studies on radiation tolerance in tardigrades have investigated limno-terrestrial species that are also highly tolerant to desiccation ( Richtersius coronifer , Milnesium tardigradum , Ramazzottius varieornatus ), the only exception being a study on the limnic species Hypsibius dujardini [7]. A common view on why tardigrades are highly tolerant to radiation is that their tolerance relies on molecular mechanisms that have evolved to allow survival under extreme but natural environmental conditions, in dry or cold environments [16].…”