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Stress Tolerance of the Endemic Antarctic Brown Alga Desmarestia Anceps to UV Radiation and Temperature Is Mediated by High Concentrations of Phlorotannins

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Stress Tolerance of the Endemic Antarctic Brown Alga Desmarestia Anceps to UV Radiation and Temperature Is Mediated by High Concentrations of Phlorotannins Photochemistry and Photobiology, 2016, 92: 455–466 Stress Tolerance of the Endemic Antarctic Brown Alga Desmarestia anceps to UV Radiation and Temperature is Mediated by High Concentrations of Phlorotannins Marıa Rosa Flores-Molina1,2*, Ralf Rautenberger2, Pamela Munoz~ 2, Pirjo Huovinen2,3 and Ivan Gomez 2,3 1Doctorado en Biologıa Marina, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile 2Instituto de Ciencias Marinas y Limnologicas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile 3Centro Fondap de Investigacion de Altas Latitudes (IDEAL), Valdivia, Chile Received 24 September 2015, accepted 19 January 2016, DOI: 10.1111/php.12580 ABSTRACT 400–700 nnm) that may impose severe limitations for photosyn- thesis. Thus, Antarctic macroalgae, are not only able to respond The endemic Antarctic brown macroalga Desmarestia anceps with the extreme seasonality in day lengths, but also exhibit a is strongly shade-adapted, but shows also a high capacity to remarkable capacity to photosynthesize efficiently at low PAR cope with different environmental stressors, e.g. UV radiation irradiances under constant low temperatures ranging between and temperature. Therefore, this species colonizes wide depth À1.8 and +2°C (reviewed in 2). gradients, which are characterized by changing environmen- Although subtidal macroalgae are usually exposed to very low tal conditions. In this study, we examine whether the differ- irradiances of solar radiation due to snow-covered sea-ice in win- ent physiological abilities allowing D. anceps to grow across a ter, many Antarctic coastal waters are highly transparent to both wide depth range is determined by high levels of phlorotan- PAR after the break-up of sea ice in spring and early summer fl nins. Photosynthesis, measured by PAM- uorometry, the before glaciers set in to melt, which results in a deep penetration contents of soluble phlorotannins, antioxidant capacities of of PAR into the water column down to 30 m (3–5). Moreover, fi eld grown were analyzed in response to different conditions at Fildes Bay on King George Island (South Shetland Islands, + of radiation (PAR and PAR UV) and temperature (2, 7 Antarctica), the penetration of ultraviolet (UV) radiation (280– ° fl and 12 C). The results show that maximal quantum of uo- 400 nm) can reach depths down to 15 m, exposing macroalgae rescence (Fv/Fm) decreased with increasing doses of UV radi- and their associated fauna and flora (i.e. epiphytes, fungi and ation, but remained unaffected by temperature. High levels bacteria) along this depth range to these potentially harmful con- fi of soluble phlorotannins were detected and con rmed by ditions (4,5). High-energy UV-B radiation (280–315 nm), which microscopic observation revealing the abundance of large is most biologically damaging, is of particular interest for marine physodes. Exposure to UV radiation and elevated tempera- biology in high latitudes because its irradiances increase under ture showed that phlorotannins were not inducible by UV stratospheric ozone depletion over Antarctica and its adjacent ° but increased at 12 C. ROS scavenging capacity was posi- regions (6–8). Scientific evidences gained throughout the past tively correlated with the contents of phlorotannins. In gen- 20 years allow to argue today that such seasonally enhanced eral, highest contents of phlorotannins were correlated with UV-B radiation plays a substantial role in the physiological and the lowest inhibition of Fv/Fm in all experimental treatments, ecological acclimation of Antarctic macroalgae, especially with highlighting the UV-protective role of these compounds in respect to photosynthetic performance, development and settle- D. anceps. ment of early life stages as well as succession processes and ver- tical zonation (2,8,9). INTRODUCTION Increasing sea surface temperatures of Antarctic waters as a result from global climate change, especially in the West Antarc- The Antarctic marine environment is characterized by extreme tic Peninsula (WAP) region, have begun to study as a factor that seasonal changes in air temperatures, light regimes and wind influences metabolic processes in the presence of UV radiation speed, as well as considerable disruptions of the upper tidal posi- (10–12). fl tions in coastal ecosystems by oating sea ice and icebergs. Due When macroalgae are exposed to both UV stress and elevated to these constraints, most of the Antarctic macroalgae grow in temperatures, their primary metabolism can be significantly fi the subtidal deeper than 5 m where they nd more stable envi- affected by structural changes or denaturation of proteins, deteri- ronmental conditions such as constant low temperatures and high oration of membrane functions, which, in turn, limits the effi- nutrient concentrations (1). However, as a consequence of inhab- ciency of photosynthetic and mitochondrial respiratory electron iting the subtidal, macroalgae adapted to predominantly occurring transport rates as well as nutrient uptake (13). The photosystem low irradiances of photosynthetically active radiation (PAR: II (PSII) reaction center complex as an essential component of the photosynthetic apparatus can be sensitive to temperatures *Corresponding author email: mrfl[email protected] (Marıa Rosa Flores- stress, resulting in a heat-induced decline in photosynthetic Molina) activity, as demonstrated by the sub-Antarctic brown macroalgae © 2016 The American Society of Photobiology 455 456 Marıa Rosa Flores-Molina et al. Durvillaea antarctica, Lessonia spicata (studied as Lessonia upper survival temperature (UST) of 11°C (31). The thermal nigrescens) and Macrocystis pyrifera (14). Moreover, the requirements of this species related to the temperature conditions heat-induced expression of genes involved in detoxification of in its subtidal habitats in Antarctic coastal ecosystems are sum- reactive oxygen species (ROS) tries to minimize oxidative dam- marized in Fig. 1. age caused as a byproduct of stress damage (15–17). To keep Desmarestia anceps has very low light demand for growth the level of damages to photosynthetic and other cellular and photosynthesis. In fact, it shows high photosynthetic efficien- components by oxidative stress low, macroalgae have different cies (i.e. the initial slopes of photosynthesis vs irradiances antioxidant mechanisms such as increasing activities of curves), high rates of dark respiration and a positive metabolic ROS-scavenging enzymes (e.g. superoxide dismutase, ascorbate carbon balance over a depth range of 20 m. These physiological peroxidase), synthesizing antioxidants such as ascorbate and adaptations allows D. anceps to colonize water depths close to glutathione, and can regenerate metabolites efficiently to avoid 30 m (3,5,31). Due to its large size of up to 4 m in length of deficiencies in antioxidant reactions (18–20). adult sporophytes (≥2 years) and dominance in Antarctic coastal Polyphenolic compounds (also known as phlorotannins) haven ecosystems, this species can be regarded as an “ecosystem engi- been shown to be highly efficient and multifunctional “antistress neer” similar to the large kelps and kelp-like brown macroalgae agents” exclusively isolated from brown macroalgae, and can from temperate regions. However, their significantly higher con- function as herbivore deterrents (20), UV-absorbing compounds centrations of phlorotannins than temperate brown macroalgae is (21,22) and even as antioxidants (23,24). It has been demon- a characteristic feature that is strongly associated with the chemi- strated that phlorotannins are important to detoxify ROS in some cal defense against several Antarctic grazers (32). The high sub-Antarctic kelps of the genera Lessonia, Durvillaea and levels of phlorotannins measured in D. anceps (≥50 mg gÀ1 dry Macrocystis under combined stress of high solar radiation and weight; DW) are apparently constitutive (i.e. constantly high) temperature (25–27). Apparently, this strategy, which is based on which raise the question to its potential as mechanism of stress the induced synthesis of phlorotannins, is crucial to brown tolerance beyond grazing alone. In this respect, Antarctica macroalgae to tolerance environmental stress and, therefore, can macroalgae that are constantly exposed to low seawater tempera- be regarded as a primary defense mechanism against episodic tures have been less studied in comparison with other photosyn- stress by elevated temperature and solar radiation. thetic organisms that experience seasonal changes in temperature. Desmarestia anceps Montagne is an endemic Antarctic brown Moreover, despite the permanently low seawater temperatures macroalga that is exclusively but widely distributed in the WAP (≤2°C) and generally low irradiances of PAR and UV radiation region and the adjacent islands, where it dominates the subtidal in the subtidal, they also require efficient mechanisms to with- benthic communities between 10 and 30 m depth (4,28,29). Due stand episodes of stress by high solar radiation, including UV to its presumable origin in the cold waters of Antarctica (30), radiation. Interactive studies between temperature and UV stress this species is strongly cold-adapted, which limits its northern that were recently carried out give first hints of a link between distribution by the temperature demands for the development and high levels of soluble phlorotannins and enhanced antioxidant growth of the sporophytes, i.e.0–5°C. Moreover, it shows a low capacities in Antarctic Desmarestiales (4,12). In the context of
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