Temporal variation of UV-B: photo-protection and photo-damage in intertidal organisms from the New Zealand coast

Abstract

Intertidal ecosystems are characterized by periodic variations in the water column throughout tidal cycles, a situation that can induce changes in the physiological balance of organisms that live there. If low tide occurs at noon, intertidal organisms can be exposed to the atmosphere, a stressful situation that can coincide with high levels of ultraviolet radiation (UV-R), increasing the risk of damage to DNA, lipids and proteins. This study intends to understand the physiological mechanisms of defense displayed by intertidal algae (Pachymenia lanciniata, Hormosira banksii and Ulva sp.) and invertebrates (Actinia tenebrosa and Diloma aethiops) during temporal variations in UV-B to avoid biomolecular damage. UV-R screening compounds, mycosporine-like amino acids (MAAs) and phenolic compounds (PC) were quantified through a 27-month field survey to understand if these secondary metabolites play a crucial role protecting the DNA against the generation of cyclobutane pyrimidine dimer (CPDs) during temporal variation of UV-B. Complementarily, levels of enzymatic and non-enzymatic antioxidants were also quantified during the 27-month field survey to determine if their synthesis responds to temporal increases in UV-R, having a more important role than screening compounds in the defense system against UV-B radiation. Finally, under controlled conditions summer and winter acclimated organisms were exposed to summer radiation levels under the following treatments (PAR (P), PAR+UVA (PA), PAR+UVA+UV-B (PAB) and PAR+UVA+UV-B enhanced 20% (PAB-20%)). The objective of this experiment was to test experimentally the effectiveness of screening compounds and antioxidant metabolisms under short time responses using long term (summer and winter) acclimated organisms. The results of this study indicate that algae showed different physiological strategies associated with the synthesis of screening compounds, mainly linked to reproductive timing than by an effect caused by UV-B radiation. Such conditions generate a lag time between the highest annual UV-B peak and the synthesis of those compounds in algae. Invertebrates also show a lag time associated with the assimilation of these compounds according to the trophic level. That lag time can leave intertidal organisms prone to generate elevated CPDs concentrations during high UV-B doses, indicating that sunscreen compounds are not efficient mechanisms to cope with increases in UV-B in the Otago Harbour. During the lag time period, antioxidant metabolism plays an important role protecting algae and invertebrates against ROS due to their fast response to UV-B radiation. High oxidative damage levels in summer can be associated with the excessive generation of ROS via photosynthesis and respiration in algae and respiration in invertebrates. Systematic differences in the biochemical composition of polyunsaturated fatty acids (PUFAs), pigments and antioxidant metabolism in algae induce differences in lipid peroxidation levels during high UV-B. In addition, elevated lipid peroxides levels in summer in invertebrates are associated with the accumulation of PUFAs during reproductive periods. Under experimental conditions, it was observed that the synthesis of enzymatic and non-enzymatic antioxidants occurs earlier than the synthesis of MAAs and PC in intertidal algae. A situation that allows saying that during elevated ROS concentration intertidal Pachymenia lanciniata, Hormosira banksii and Ulva sp. reallocates more resources into the antioxidant metabolism rather than to the synthesis of MAAs and PC. Reduced levels of oxidative damage in Diloma aethiops is conferred by the physical barrier effect that the shell confers against the generation of ROS via UV-R, whereas Actinia tenebrosa are completely exposed to UV-R showing elevated oxidative damage. In addition, winter acclimated organisms showed an increased susceptibility to PA, PAB and PAB-20%, whereas summer acclimated organisms showed susceptibility to PAB-20%. Thus it is possible to conclude that antioxidant metabolism play a pivotal role in the defense line against the noxious effects of UV-R and its activity must be complemented by the action of screening metabolites to make the protection system more efficient. Independently of the strategy used by invertebrates of algae, the metabolic cost of defences against UV-R is energetically high and must be carried out during constant energetic demands associated with biomolecular repair processes and on-going metabolism.