Solar UVB-induced DNA damage and photoenzymatic DNA repair in antarctic zooplankton

Abstract

The detrimental effects of elevated intensities of mid-UV radiation (UVB), a result of stratospheric ozone depletion during the austral spring, on the primary producers of the Antarctic marine ecosystem have been well documented. Here we report that natural populations of Antarctic zooplankton also sustain significant DNA damage [measured as cyclobutane pyrimidine dimers (CPDs)] during periods of increased UVB f lux. This is the first direct evidence that increased solar UVB may result in damage to marine organisms other than primary producers in Antarctica. The extent of DNA damage in pelagic icefish eggs correlated with daily incident UVB irradiance, ref lecting the difference between acquisition and repair of CPDs. Patterns of DNA damage in fish larvae did not correlate with daily UVB f lux, possibly due to different depth distributions and͞or different capacities for DNA repair. Clearance of CPDs by Antarctic fish and krill was mediated primarily by the photoenzymatic repair system. Although repair rates were large for all species evaluated, they were apparently inadequate to prevent the transient accumulation of substantial CPD burdens. The capacity for DNA repair in Antarctic organisms was highest in those species whose early life history stages occupy the water column during periods of ozone depletion (austral spring) and lowest in fish species whose eggs and larvae are abundant during winter. Although the potential reduction in fitness of Antarctic zooplankton resulting from DNA damage is unknown, we suggest that increased solar UV may reduce recruitment and adversely affect trophic transfer of productivity by affecting heterotrophic species as well as primary producers.

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

“…When photoreactivation rate is compared among the three species across experimental temperatures (32°C to -1.9°C), photoreactivation rates decrease with a Q 10 =1.39 (Fig.·5). Observations by Malloy et al, however (Malloy et al, 1997), suggest that there has been temperature compensation across broader phylogenetic comparisons, with rates in Antarctic krill and pelagic fish comparable with warmer water fishes. Photolyases are an ancient enzyme evolutionarily, and have been shown to be highly conserved structurally and functionally amongst distantly related organisms (Sancar, 1990).…”

“…We estimated CPD photorepair rate constants (k) in echinoid embryos of between k=0.33 and 0.125·h -1 , equating to a time to 50% repair of 0.6 to 2.1·h and time to repair 90% of 3.6 to 13.6·h. These rates encompass previous estimates of CPD repair rate constants (reported as relative photorepair rate, R) in Antarctic [R=0.57 and 0.93 (Malloy et al, 1997) (Mitchell et al, 1986)], but lower than rates observed in the variable platyfish, Xiphophorous variatus [RϷ1.6 (Mitchell et al, 1993)]. Time to repair CPDs expressed as a percentage for these organisms as well as for E. coli and mammalian cells (Table·4) are variable, with time to repair 50% ranging from 25 to 40·min in E. coli (Koehler et al, 1996), 1·h in the vascular plant Arabidopsis thaliana (Pang and Hays, 1991), to 6·h in mammalian cells (Mellon et al, 1986).…”

“…The comparison suggests instead, that rate is more strongly influenced by life history or environment. Indeed, Malloy et al concluded from their comparison of repair in Antarctic fish that repair rate might be related to vertical distribution in the water column and ambient UV-R (Malloy et al, 1997).…”

“…Previous research has shown that CPD repair is primarily carried out by photoreactivation (Malloy et al, 1997;Häder and Sinha, 2005) and occurs in the embryos of a number of sea urchin species (Marshak, 1949;Wells and Giese, 1950;Ejima et al, 1984;Akimoto and Shiroya, 1986). In our study, we established that in the three species and in three developmental stages of Sterechinus, photoreactivation was the primary means of removing CPDs, and was effective in repairing all CPDs in less than 24·h (Fig.·7).…”

“…Marine organisms can prevent this damage by passive methods with relatively low energetic costs such as sunscreens and non-enzymatic anti-oxidants (Dunlap et al, 2000), or by active, energetically costly, mechanisms such as antioxidant enzymes, photoreactivation and dark-excision DNA repair (Kim and Sancar, 1993;Malloy et al, 1997;Mitchell and Hartman, 1990). Three important points relevant to Antarctic embryos with very slow metabolism are: (i) the metabolic costs of active UV-R mitigation could result in reduced rates of repair; (ii) the continuously cold Antarctic waters would result in reduced activity of enzymes involved in UV-R mitigation if no cold-adaptation has occurred (Somero, 1995;Marshall, 1997) and; (iii) the low UV-R environment in the past may not have imposed selective pressures to evolve efficient UV-R mitigation strategies.…”