Analysis of DNA Repair and Protection in the Tardigrade Ramazzottius varieornatus and Hypsibius dujardini after Exposure to UVC Radiation

Abstract

Tardigrades inhabiting terrestrial environments exhibit extraordinary resistance to ionizing radiation and UV radiation although little is known about the mechanisms underlying the resistance. We found that the terrestrial tardigrade Ramazzottius varieornatus is able to tolerate massive doses of UVC irradiation by both being protected from forming UVC-induced thymine dimers in DNA in a desiccated, anhydrobiotic state as well as repairing the dimers that do form in the hydrated animals. In R. varieornatus accumulation of thymine dimers in DNA induced by irradiation with 2.5 kJ/m2 of UVC radiation disappeared 18 h after the exposure when the animals were exposed to fluorescent light but not in the dark. Much higher UV radiation tolerance was observed in desiccated anhydrobiotic R. varieornatus compared to hydrated specimens of this species. On the other hand, the freshwater tardigrade species Hypsibius dujardini that was used as control, showed much weaker tolerance to UVC radiation than R. varieornatus, and it did not contain a putative phrA gene sequence. The anhydrobiotes of R. varieornatus accumulated much less UVC-induced thymine dimers in DNA than hydrated one. It suggests that anhydrobiosis efficiently avoids DNA damage accumulation in R. varieornatus and confers better UV radiation tolerance on this species. Thus we propose that UV radiation tolerance in tardigrades is due to the both high capacities of DNA damage repair and DNA protection, a two-pronged survival strategy.

Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade

“…Tardigrades accumulate extensive DNA double-strand breaks with prolonged desiccation and when exposed to high levels of radiation (6,18,19). A number of protein families involved in DNA repair have been expanded in tardigrades (Dataset S4), and this expansion is due to the acquisition of foreign DNA in many cases.…”

“…1A) are animals that are known for anhydrobiosis (surviving life without water). Tardigrades survive several additional stresses normally thought to be incompatible with life (1, 2), including extreme temperatures (−272 to 151°C) (3,4), radiation intensities orders of magnitude greater than humans can withstand (5,6), incubation in organic solvents (7), and extremes of pressure (8). Tardigrades are the only animal known to survive exposure to the vacuum of space (8).…”

Tolerance to Gamma Radiation in the Marine Heterotardigrade, Echiniscoides sigismundi

“…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].…”

No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini

“…All are small (tardigrades are usually classified in the meiofauna) and are found in sediments and on vegetation from the Antarctic to the Arctic, from mountain ranges to the deep sea, and in marine and fresh water environments. Their dispersal may be associated with the ability of many (but not all) species to enter cryptobiosis, losing almost all body water, and resisting extremes of temperature, pressure, and desiccation (6)(7)(8)(9), deep space vacuum (10), and irradiation (11). Interest in tardigrades focuses on their utility as environmental and biogeographic markers, the insight their cryptobiotic mechanisms may yield for biotechnology and medicine, and exploration of their development compared with other Ecdysozoa, especially Nematoda and Arthropoda.…”