DNA photorepair in echinoid embryos: effects of temperature on repair rate in Antarctic and non-Antarctic species

Abstract

Over recent geological time the Antarctic marine system has been a relatively low ultraviolet radiation (UV-R) environment because of its polar location, high atmospheric ozone concentrations, and extensive seasonal covering by relatively opaque, and highly reflective, sea ice. Recent increases in ultraviolet-B radiation (280-315·nm) due to stratospheric ozone depletion have highlighted the susceptibility of marine ecosystems to this important abiotic factor (Smith et al., 1992;Karentz, 1994;Smith and Cullen, 1995). The occurrence of the spring ozone hole coincides with the development of embryos of many Antarctic marine invertebrates that may be susceptible to the effects of UV-R because of their small size, lack of a protective tegument, and high rate of cell division (Johnsen and Widder, 2001). Antarctic embryos may be especially vulnerable because they have unique physiological adaptations to survive the cold, food-poor Antarctic waters (cf. Marsh et al., 2001).Our recent observations confirm that Antarctic marine larvae are very sensitive to UV-R (Lesser et al., 2004). Echinoid embryos exposed to ambient UV-R under annual Antarctic sea ice (a low UV-R environment with irradiances р1% of surface irradiances), exhibited significantly higher rates of mortality, abnormal development (Ϸ30-50%), and DNA damage than embryos exposed concurrently but under a UV-R filter. Biological weighting functions for DNA damage and survival To determine if an Antarctic species repairs DNA at rates equivalent to warmer water equivalents, we examined repair of UV-damaged DNA in echinoid embryos and larvae. DNA repair by photoreactivation was compared in three species Sterechinus neumayeri (Antarctica), Evechinus chloroticus (New Zealand) and Diadema setosum (Tropical Australia) spanning a latitudinal gradient from polar (77.86°S) to tropical (19.25°S) environments. We compared rates of photoreactivation as a function of ambient and experimental temperature in all three species, and rates of photoreactivation as a function of embryonic developmental stage in Sterechinus. DNA damage was quantified from cyclobutane pyrimidine dimer (CPD) concentrations and rates of abnormal embryonic development. This study established that in the three species and in three developmental stages of Sterechinus, photoreactivation was the primary means of removing CPDs, was effective in repairing all CPDs in less than 24·h, and promoted significantly higher rates of normal development in UV-exposed embryos. CPD photorepair rate constant (k) in echinoid embryos ranged from 0.33 to 1.25·h -1 , equating to a time to 50% repair of between 0.6 and 2.1·h and time to 90%repair between 3.6 and 13.6·h. We observed that experimental temperature influenced photoreactivation rate. In Diadema plutei, the photoreactivation rate constant increased from k=0.58·h -1 to 1.25·h -1 , with a Q 10 =2.15 between 22°C and 32°C. When compared among the three species across experimental temperatures (-1.9 to 32°C), photoreactivation rates vary with a Q 10 =1.39. Photoreactivati...

In situ rates of DNA damage and abnormal development in Antarctic and non-Antarctic sea urchin embryos

“…In contrast to temperate and tropical species, the Antarctic embryos accumulated a higher number of CPDs during early development, and were also found to have the highest rates of abnormal embryo development when exposed to both UV-B and UV-A. Lamare et al (2006) showed that DNA repair is slower and likely due to the lack of temperature compensation in the enzyme mediated photorepair process in S. neumayeri. The greater DNA damage in Antarctica may in essence be the result of cold sea temperatures, which while not effecting initial CPD formation (the rate of which should be relatively temperature independent), substantially slows metabolic processes such as DNA repair.…”

“…Methods are described in detail in Lamare et al (2006). TDM-2 primary monoclonal antibodies specific to CPDs were supplied by Medical and Biological Laboratories, Nagoya, Japan.…”

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.…”

Molecular and sensory mechanisms to mitigate sunlight-induced DNA damage in treefrog tadpoles

“…For instance, the photorepair in coral planulae is very efficient, as it repairs 50% of UVB-induced DNA damage in 23 min (Reef et al, 2009). Additionally, the photorepair of some species of echinoid embryos removes 50% of CPDs in 0.6 h (Lamare et al, 2006). In fishes, this DNA repair pathway also operates more quickly than nucleotide excision repair (NER), removing damage on a scale of minutes compared with hours or days for NER (Kienzler et al, 2013a).…”