Temperature Effects on Survival and DNA Repair in Four Freshwater Cladoceran Daphnia Species Exposed to UV Radiation

Abstract

The biological responses of four freshwater daphniid species, Daphnia middendorffiana, D. pulicaria, D. pulex and D. parvula, to a single acute dose of ultraviolet B radiation (UVB) were compared. In addition to survival, we compared the induction of DNA damage (i.e. cyclobutane pyrimidine dimers) between species as well as the ability to repair this damage in the presence or absence of photoreactivating light. All four species showed high levels of shielding against DNA damage when compared to damage induced in purified DNA dosimeters at the same time and dose. Significant variation in survival was observed between species depending on temperature and light conditions. Contrary to our expectations, all species showed significantly higher survival and light-dependent DNA damage removal rates at 10°C compared to 20°C, suggesting that the enhanced rate of photoenzymatic repair (PER) at the lower temperature contributed significantly to the recovery of these organisms from UVB. PER was highly effective in promoting survival of three of the four species at 10°C, but at 20°C it was only partially effective in two species, and ineffective in two others. None of the species showed significant dark repair at 20°C and only D. pulicaria showed a significant capacity at 10°C. Two species, D. middendorffiana and D. pulex, showed some short-term survival at 10°C in absence of PER despite their inability to repair any appreciable amount of DNA damage in the dark. All species died rapidly at 20°C in absence of PER, as predicted from complete or near-absence of nucleotide excision repair (NER). Overall, the protective effects of tissue structure and pigmentation were similar in all Daphnia species tested and greatly mitigated the absorption of UVB by DNA and its damaging effects. Surprisingly, the visibly melanotic D. middendorffiana was not better shielded from DNA damage than the three non-melanotic species, and in fact suffered the highest damage rates. Melanin content in this species was not temperature dependent under the experimental growth conditions, and so did not contribute to temperature-dependent responses. It is evident that different species within the same genus have developed diverse biological responses to UVB. Our data strongly suggest that DNA damage is lethal to Daphnia and that photoenzymatic repair is the primary mechanism for removing these lesions. In the absence of light, few species are capable of removing any DNA damage. Surprisingly, the single species in which significant excision repair was detected did so only at reduced temperature. This temperature-dependence of excision repair is striking and may reflect adaptations of certain organisms to stress in a complex and changing environment.

Drivers of amphibian declines: effects of ultraviolet radiation and interactions with other environmental factors

“…Only the activity of the antioxidant enzyme catalase has been shown not to be thermally sensitive in response to UVR exposure in L. peronii tadpoles [72]. However, the DNA repair mechanisms of enzymatic photoreactivation (EPR) and nucleotide excision repair (NER) have been shown to increase with increasing temperature in ciliates [115], freshwater crustaceans [116], marine macroalgae [117], tobacco cells [118] and echinoid embryos [119], however, Connelly et al [120] found the opposite to be true in Daphnia. The photoprotective mechanism of ROS reduction by enzymatic antioxidant activity has also been found to be thermally sensitive in summer-caught mosquito fish Gambusia holbrooki exposed to UVR [39].…”

“…Kazerouni et al [39] found that the activities of superoxide dismutase and catalase were highest in fish acclimated to the average environmental temperature of 28°C, but was reduced in fish acclimated to lower and higher temperatures (18°C and 32°C). Importantly, the improved efficiency of EPR, NER and antioxidant activity due to changes in temperature has been found to reduce the negative effects associated with UVR exposure on development, survival, metabolic rate and locomotor performance [39,119,120]. Given that EPR, NER and antioxidant activity are thermally sensitive in other organisms, it seems likely that these physiological UVR defences are also thermally sensitive in amphibians.…”

Direct Effects of UV-B Radiation on the Freshwater Heterotrophic NanoflagellateParaphysomonassp

“…Although PER is widespread taxonomically (16), its importance relative to dark repair is highly variable for different organisms. PER has been shown to be a particularly important mechanism of DNA repair in several species of amphibians (2), zooplankton (7,12,14), protists (26,31), and bacteria (22). Zenoff et al (39) found several strains of aquatic bacteria with various degrees of reliance on PER and no obvious use of NER, although Cytophaga sp.…”

“…An overall reduced metabolism at the cooler temperature could have contributed to these differences; however, it seems likely that the photolyase enzyme itself was less efficient at 15°C. The interaction of temperature with DNA repair is known for several other taxa exposed to UV-B, including a red alga, a ciliate, a rotifer, and several crustacean zooplankton species (7,13,21,26,36).…”

The impact of UVB radiation on the glycoprotein glue of orb-weaving spider capture thread

“…Marine and terrestrial organisms have adapted to prevent and cope with such UVR exposure and damage. These adaptations can be behavioral, such as moving into the shade (Gleason et al, 2006;Ma et al, 2013), physiological, such as absorptive pigmentation like melanin (Singaravelan et al, 2008) and mycosporine-like amino acids (MAAs) (Kuffner, 2002;Hylander and Hansson, 2013), or biochemical such as molecular repair (Carlson and Smith, 1981;Connelly et al, 2009) and antioxidants (Swindells and Rhodes, 2004;Hudelson, 2011).…”