Tolerance to Gamma Radiation in the Marine Heterotardigrade, Echiniscoides sigismundi

Abstract

Tardigrades belong to the most radiation tolerant animals on Earth, as documented by a number of studies using both low-LET and high-LET ionizing radiation. Previous studies have focused on semi-terrestrial species, which are also very tolerant to desiccation. The predominant view on the reason for the high radiation tolerance among these semi-terrestrial species is that it relies on molecular mechanisms that evolved as adaptations for surviving dehydration. In this study we report the first study on radiation tolerance in a marine tardigrade, Echiniscoides sigismundi. Adult specimens in the hydrated active state were exposed to doses of gamma radiation from 100 to 5000 Gy. The results showed little effect of radiation at 100 and 500 Gy but a clear decline in activity at 1000 Gy and higher. The highest dose survived was 4000 Gy, at which ca. 8% of the tardigrades were active 7 days after irradiation. LD50 in the first 7 days after irradiation was in the range of 1100–1600 Gy. Compared to previous studies on radiation tolerance in semi-terrestrial and limnic tardigrades, Echiniscoides sigismundi seems to have a lower tolerance. However, the species still fits into the category of tardigrades that have high tolerance to both desiccation and radiation, supporting the hypothesis that radiation tolerance is a by-product of adaptive mechanisms to survive desiccation. More studies on radiation tolerance in tardigrade species adapted to permanently wet conditions, both marine and freshwater, are needed to obtain a more comprehensive picture of the patterns of radiation tolerance.

Modelling extreme desiccation tolerance in a marine tardigrade

“…Specifically, the semi-terrestrial eutardigrade, Ramazzottius oberhaeuseri , tolerates desiccation for 1192 days with a mean activity recovery of 21.7%, whereas a mean activity of 9.9% was recorded for the semi-terrestrial heterotardigrade, Echiniscus spp., following 706 days of desiccation 14 . A similar pattern revealing a somewhat lower tolerance in Echiniscoides as compared to semi-terrestrial tardigrades was observed in a study on tolerance to gamma radiation 35 . The latter may simply reflect a variation in the tolerance level of specific tardigrade species, but, importantly, could also support the argument that electrolyte solutions have a detrimental effect on the ability to recover from extreme stress, as previously reported for semi-terrestrial species 36 .…”

“…Importantly, at the population level, E. sigismundi is likely able to survive >1 year of quiescence as only a few survivors would be needed to re-establish the population. As holds for many of the extreme adaptations reported among tardigrades 16 , 35 , 37 , 38 , the time endured in the quiescent state seems as a bit of a paradox, as the tardigrades under natural conditions would not be desiccated for such a long period of time 39 .…”

Radiation Tolerance in Tardigrades: Current Knowledge and Potential Applications in Medicine

“…More detailed summaries of dose-response studies in tardigrades can be found elsewhere [16,29]. In the only marine species investigated, Echiniscoides sigismundi , tolerance to γ-ray was clearly lower, with an LD50 estimate around 1.5 kGy 7 days post-irradiation [30]. The similar dose-response in desiccated and hydrated tardigrades (Figure 2) seems to be a general feature, which is unexpected given that the indirect effects of ionizing radiation are expected to be much higher in the presence of water [31].…”

“…An exception seems to be the marine heterotardigrade E. sigismundi , which was reported to lack pathways for non-homologous end joining (c-NHEJ), one of the major pathways for repair of DNA double-strand breaks besides homologous recombination (HR) [69]. This species is tolerant to rapid desiccation [74], but seems to be less tolerant to long-term anhydrobiosis compared to semi-terrestrial tardigrades [75], and as mentioned above, it also has a lower tolerance to ionizing radiation [30]. Whether the lower radiation tolerance in E. sigismundi is related to the observed difference in DNA repair pathways remains to be investigated.…”

Multiomics study of a heterotardigrade,Echinisicus testudo, suggests convergent evolution of anhydrobiosis-related proteins in Tardigrada

“…However, many limno-terrestrial tardigrades are able to enter an ametabolic state, known as anhydrobiosis, when they face desiccation, and these organisms can subsequently tolerate almost complete water loss while being able to return to their natural active state when rehydrated [1][2][3] . In anhydrobiosis, tardigrades are capable of tolerating many extreme environments, such as high and low temperatures 4,5 , space vacuum 6 , high pressure 7 , and high concentrations of organic solvent 8 , as well as insults from ultraviolet rays and over 4,000 Gy of gamma radiation [9][10][11] .…”