Cooler temperatures slow the repair of DNA damage in tadpoles exposed to ultraviolet radiation: Implications for amphibian declines at high altitude

Abstract

Ultraviolet B radiation (UVBR) damages the DNA of exposed cells, causing dimers to form between adjacent pyrimidine nucleotides. These dimers block DNA replication, causing mutations and apoptosis. Most organisms utilize biochemical or biophysical DNA repair strategies to restore DNA structure; however, as with most biological reactions, these processes are likely to be thermally sensitive. Tadpoles exposed to elevated UVBR at low environmental temperatures have significantly higher rates of mortality and developmental deformities compared with tadpoles exposed to the same levels of UVBR at higher environmental temperatures. We hypothesized that low environmental temperatures impair the primary enzymatic (photolyase) DNA repair pathway in amphibians, leading to the accumulation of DNA damage. To test this hypothesis, we compared DNA repair rates and photolyase gene expression patterns in Limnodynastes peronii. Tadpoles were acutely exposed to UVBR for 1 hr at either 20 or 30°C, and we measured DNA damage and photolyase expression levels at intervals following this exposure. Temperature had a significant effect on the rate of DNA repair, with repair at 30°C occurring twice as fast as repair at 20°C. Photolyase gene expression (6‐4 PP and CPD) was significantly upregulated by UVBR exposure, with expression levels increasing within 6 hr of UVBR exposure. CPD expression levels were not significantly affected by temperature, but 6‐4 PP expression was significantly higher in tadpoles in the 30°C treatment within 12 hr of UVBR exposure. These data support the hypothesis that DNA repair rates are thermally sensitive in tadpoles and may explain why enigmatic amphibian declines are higher in montane regions where UVBR levels are naturally elevated and environmental temperatures are lower.

HREM, RNAseq and cell-cycle analyses reveal the role of the G2/M-regulatory protein, Wee1, on the survivability of chicken embryos during diapause.

“…Thus, the premature termination of the repair process, may have increased the number of TUNEL-positive cells in 12°C-diapaused embryos. Interestingly, it has been previously shown that DNA damage is increased at low temperature in frog tadpole, fish and shrimps [70–73]. DNA damage activates the ATM/ATR DNA damage response mechanisms [74–76], found in tumors and cancerous cells, which in turn induces the expression of Wee1 [77,78], resulting in cell cycle arrest at the G2/M phase [66].…”

“…shown that DNA damage is increased at low temperature in frog tadpole, fish and shrimps [70][71][72][73]. DNA damage activates the ATM/ATR DNA damage response mechanisms [74][75][76], found in tumors and cancerous cells, which in turn induces the expression of Wee1 [77,78], resulting in cell cycle arrest at the G2/M phase [66].…”

Biological impact of ultraviolet-B radiation on spider mites and its application in integrated pest management

“…Photoreactivation via repair of DNA lesions such as CPDs and 6-4 PPs via PER is essential, and the reactivation system is present in a wide range of organisms, including bacteria (Ikenaga et al 1970;Peccia and Hernandez 2001), rotifers (Grad et al 2003), crustaceans (Connelly et al 2009;Damkaer and Dey 1983;Grad and Williamson 2001), algae (Pakker et al 2000;Pescheck 2019), plants (Hada et al 2003;Kaiser et al 2009;Manova et al 2016;Takahashi et al 2002), amphibians (Blaustein et al 1994;Morison et al 2020), and fishes (Applegate and Ley 1988;Lawrence et al 2020;Mitchell et al 2009;Wiegand et al 2004), but not in placental mammals, which may rely on other repair systems: base excision repair, NER, and so on (Sinha and Häder 2002). In spider mites, Santos (2005) observed photoreactivation of UV-B damage in T. urticae, the mortality rate of T. urticae adult females irradiated with UV-B at 46.8 kJ/m 2 was reduced from 46% (when kept in the dark after UV-B irradiation) to 26% with VIS illumination after UV-B irradiation.…”

Molecular insights into the ecology of a psychrotolerant Pseudomonas syringae

“…At low temperature, physiologically active microbes are prone to DNA damage (Mangoli et al ., 2014) and the efficiency of DNA repair process is reduced (Morison et al ., 2020). Various intrinsic and extrinsic factors can cause increased DNA damage at low temperature, including ultra‐violet radiation (UV) and reactive oxygen species (Lisowska et al ., 2018; Morison et al ., 2020). The majority of DNA lesions in a living cell are mediated by oxidative damage, arising from hydroxyl radicals (Storz and Imlay, 1999).…”