Abstract
Space exposure experiments from the last 15 years have unexpectedly shown that several terrestrial organisms, including some multi-cellular species, are able to survive in open space without protection. The robustness of bdelloid rotifers suggests that these tiny creatures can possibly be added to the still restricted list of animals that can deal with the exposure to harsh condition of space. Bdelloids are one of the smallest animals on Earth. Living all over the world, mostly in semi-terrestrial environments, they appear to be extremely stress tolerant. Their desiccation tolerance at any stage of their life cycle is known to confer tolerance to a variety of stresses including high doses of radiation and freezing. In addition, they constitute a major scandal in evolutionary biology due to the putative absence of sexual reproduction for at least 60 million years. Adineta vaga, with its unique characteristics and a draft genome available, was selected by ESA (European Space Agency) as a model system to study extreme resistance of organisms exposed to space environment. In this manuscript, we documented the resistance of desiccated A. vaga individuals exposed to increasing doses of X-ray, protons and Fe ions. Consequences of exposure to different sources of radiation were investigated in regard to the cellular type including somatic (survival assay) and germinal cells (fertility assay). Then, the capacity of A. vaga individuals to repair DNA DSB induced by different source of radiation was investigated. Bdelloid rotifers represent a promising model in order to investigate damage induced by high or low LET radiation. The possibility of exposure both on hydrated or desiccated specimens may help to decipher contribution of direct and indirect radiation damage on biological processes. Results achieved through this study consolidate our knowledge about the radioresistance of A. vaga and improve our capacity to compare extreme resistance against radiation among living organisms including metazoan.
Highlights
The exposition of cells to ionizing radiations (IR) generates a succession of physical, chemical and biological processes that differ in time, spatial and energy-scale leading to a cellular response complicated to predict (Joiner and van der Kogel, 2018)
DNA repair kinetics suggest that most DNA damage induced by radiation are repaired within 24 h independently of the radiation source or on the reproductive capacity. These results suggest that the DNA repair kinetic taking place in somatic cells of irradiated A. vaga individuals appeared to be insensitive to the complexity of damage induced by low vs. high Linear Energy Transfer (LET) radiation exposures
The robustness of bdelloid rotifers against multiple stresses coupled with their desiccation tolerance at any stage of their life cycle prone them to the short list of animals that can be used as model systems to study how life can be adapted and could evolve in extra-terrestrial environments (Jönsson et al, 2008; Vukich et al, 2012; Rabbow et al, 2015)
Summary
The exposition of cells to ionizing radiations (IR) generates a succession of physical, chemical and biological processes that differ in time, spatial and energy-scale leading to a cellular response complicated to predict (Joiner and van der Kogel, 2018). High-Z charged particles (such as Fe ions) are high LET particles that will produce dense ionizations along their path while photons (like X-rays) which produce sparse ionizations are considered as low LET IR (Joiner and van der Kogel, 2018; Hagiwara et al, 2019). Complex DNA damages including clustered double strand breaks (DSBs) are preferentially created following high-LET exposition resulting in a poor survival of irradiated organisms (Semenenko and Stewart, 2004). The health risks from exposure to terrestrial radiations (electrons and photons) are well known, the ones associated to heavy ions particles (HZE) remain poorly understood since they are only naturally present in space. Bdelloid rotifers are known to survive high doses of high and low LET ionizing radiation (Gladyshev and Meselson, 2008; Hespeels et al, 2014; Jönsson and Wojcik, 2017), making them a new, suitable model system for space research
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