Extreme resistance of bdelloid rotifers to ionizing radiation

Abstract

Rotifers of class Bdelloidea are common invertebrate animals with highly unusual characteristics, including apparently obligate asexuality, the ability to resume reproduction after desiccation at any life stage, and a paucity of transposable genetic elements of types not prone to horizontal transmission. We find that bdelloids are also extraordinarily resistant to ionizing radiation (IR). Reproduction of the bdelloids Adineta vaga and Philodina roseola is much more resistant to IR than that of Euchlanis dilatata, a rotifer belonging to the desiccation-intolerant and facultatively sexual class Monogononta, and all other animals for which we have found relevant data. By analogy with the desiccation-and radiationresistant bacterium Deinococcus radiodurans, we suggest that the extraordinary radiation resistance of bdelloid rotifers is a consequence of their evolutionary adaptation to survive episodes of desiccation encountered in their characteristic habitats and that the damage incurred in such episodes includes DNA breakage that is repaired upon rehydration. Such breakage and repair may have maintained bdelloid chromosomes as colinear pairs and kept the load of transposable genetic elements low and may also have contributed to the success of bdelloid rotifers in avoiding the early extinction suffered by most asexuals.desiccation ͉ DNA repair ͉ asexual reproduction ͉ anhydrobiosis

Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

“…Such persistence and diversification of an ameiotic clade of animals are in contradiction with the supposed long-term disadvantages of asexuality, making bdelloids an 'evolutionary scandal' 5 . Another unusual feature of bdelloid rotifers is their extreme resistance to desiccation at any stage of their life cycle 6 , enabling these microscopic animals to dwell in ephemeral freshwater habitats such as mosses, lichens and forest litter; this ability is presumably the source of their extreme resistance to ionizing radiation 7 .…”

Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans

“…This remarkable robustness is embodied in the exceptional ability to repair hundreds of DNA double-strand breaks (DSB) generated by high doses of ionizing radiation (1). Remarkably, ionizing radiation-induced DSB are generated with equal efficiency in all prokaryotic and eukaryotic cells examined (~0.005 DSB/Mbase/Gy irradiation) (2,3). Thus, high radiation resistance is associated with high efficacy of DNA repair.…”

General environmental heterogeneity as the explanation of sexuality? Comparative study shows that ancient asexual taxa are associated with both biotically and abiotically homogeneous environments

“…Alternative ways of exchange of genetic information could theoretically substitute sexual reproduction and thus were repeatedly proposed as the key adaptation to asexuality (Boschetti, Pouchkina‐Stantcheva, Hoffmann, & Tunnacliffe, 2011; Butlin, Schön, & Griffiths, 1998; Debortoli et al., 2016; Gladyshev & Meselson, 2008; Schwander, 2016). However, we identified this factor only once in the AAs included in our study (i.e., in one of eight cases), namely in Bdelloidea that experience intensive horizontal gene transfer (Boschetti et al., 2011; Debortoli et al., 2016; Gladyshev & Meselson, 2008).…”

“…However, we identified this factor only once in the AAs included in our study (i.e., in one of eight cases), namely in Bdelloidea that experience intensive horizontal gene transfer (Boschetti et al., 2011; Debortoli et al., 2016; Gladyshev & Meselson, 2008). Another mechanism of genetic exchange, parasexuality (sensu Pontecorvo, 1954), was proposed in some contested ancient asexuals—Glomales (Croll & Sanders, 2009), Tricholomataceae and Lepiotaceae (Mikheyev, Mueller, & Abbot, 2006), and certain protists (Birky, 2009).…”