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Effects of increased seawater temperature on UV tolerance of Antarctic marine macroalgae

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Abstract

Cold-adapted Antarctic marine macroalgae have different physiological strategies to tolerate the ultraviolet (UV) radiation at low seawater temperatures around 0 °C. The warming of Antarctica’s coasts driven by global climate change may alter the physiology such to influence their UV tolerance. This study examined the interactive effects of different seawater temperatures (2 vs. 7 °C) and UV radiation on the physiological performance (primary photochemistry: F v/F m, soluble and insoluble phlorotannins, radical scavenging capacity) of seven macroalgae, which are dominant in Antarctic coastal ecosystems. Four brown and three red macroalgae, collected from Fildes Bay (King George Island, South Shetland Islands) in January/February, were exposed to 6 h of UV/temperature stress, followed by a 16-h recovery. The brown macroalgae Desmarestia menziesii and Ascoseira mirabilis showed the highest UV tolerance at 2 °C, followed by Desmarestia anceps, and the rhodophytes Iridaea cordata, Trematocarpus antarcticus, and Palmaria decipiens. Himantothallus grandifolius (Phaeophyceae) was sensitive to UV radiation at 2 °C. At 7 °C, UV tolerance was improved in UV-sensitive macroalgae probably due to a more efficient damage repair of the photosynthetic apparatus. Temperature, however, did not modulate UV tolerance in D. anceps, indicating an UV-sensitive repair process. Constitutively, high contents of soluble and insoluble phlorotannins and radical scavenging capacities remained unchanged in endemic Desmarestiales. UV induction of soluble phlorotannins along with an increased radical scavenging capacity can be responsible for A. mirabilis’ high UV tolerance. This study suggests that UV tolerance in macroalgae, which are sensitive to UV radiation at 2 °C, is modulated by temperature. Enhanced UV tolerance at 7 °C can be apparently ascribed to the stimulation of damage repair of the photosynthetic apparatus rather than to an enhanced UV screening or radical scavenging.

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References

  • Abdala-Díaz RT, Cabello-Pasini A, Márquez-Garrido E, Figueroa FL (2014) Intra-thallus variation of phenolic compounds, antioxidant activity, and phenolsulphatase activity in Cystoseira tamariscifolia (Phaeophyceae) from southern Spain. Cienc Mar 40:1–10

    Article  Google Scholar 

  • Agati G, Azzarello E, Pollastri S, Tattini M (2012) Flavonoids as antioxidants in plants: Location and functional significance. Plant Sci 196:67–76

    Article  CAS  Google Scholar 

  • Arnold TM, Targett NM (2003) To grow and defend: Lack of tradeoffs for brown algal phlorotannins. Oikos 100:406–408

    Article  Google Scholar 

  • Bischof K, Hanelt D, Wiencke C (1998) UV-radiation can affect depth-zonation of Antarctic macroalgae. Mar Biol 131:597–605

    Article  Google Scholar 

  • Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder UH, Roleda MY, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Biotechnol 5:141–166

    Article  CAS  Google Scholar 

  • Bouchard JN, Campbell DA, Roy S (2005a) Effects of UV-B radiation on the D1 protein repair cycle of natural phytoplankton communities from three latitudes (Canada, Brazil, and Argentina). J Phycol 41:273–286

    Article  CAS  Google Scholar 

  • Bouchard JN, Roy S, Ferreyra G, Campbell DA, Curtosi A (2005b) Ultraviolet-B effects on photosystem II efficiency of natural phytoplankton communities from Antarctica. Polar Biol 28:607–618

    Article  Google Scholar 

  • Bouchard JN, Roy S, Campbell DA (2006) UVB effects on the photosystem II-D1 protein of phytoplankton and natural phytoplankton communities. Photochem Photobiol 82:936–951

    Article  CAS  Google Scholar 

  • Brey L (2009) Acclimation of kelp photosynthesis to seasonal changes in the underwater radiation regime of an Arctic fjord system. Dissertation, University of Bremen

  • Cruces E, Huovinen P, Gómez I (2012) Phlorotannin and antioxidant responses upon short-term exposure to UV radiation and elevated temperature in three South Pacific kelps. Photochem Photobiol 88:58–66

    Article  CAS  Google Scholar 

  • Cruces E, Huovinen P, Gómez I (2013) Interactive effects of UV radiation and enhanced temperature on photosynthesis, phlorotannin induction and antioxidant activities of two sub-Antarctic brown algae. Mar Biol 160:1–13

    Article  CAS  Google Scholar 

  • Eggert A (2012) Seaweed responses to temperature. In: Wiencke C, Bischof K (eds) Seaweed biology. Novel insights into ecophysiology, ecology and utilization. Ecol Stud 219, Springer, Berlin, pp 47–66

  • Fairhead VA, Amsler CD, McClintock JB, Baker BJ (2005) Variation in phlorotannin content within two species of brown macroalgae (Desmarestia anceps and D. menziesii) from the Western Antarctic Peninsula. Polar Biol 28:680–686

    Article  Google Scholar 

  • Fairhead VA, Amsler CD, McClintock JB, Baker BJ (2006) Lack of defense or phlorotannin induction by UV radiation or mesograzers in Desmarestia anceps and D. menziesii (Phaeophyceae). J Phycol 42:1174–1183

    Article  CAS  Google Scholar 

  • Fredersdorf J, Müller R, Becker S, Wiencke C, Bischof K (2009) Interactive effects of radiation, temperature and salinity on different life history stages of Arctic kelp Alaria esculenta (Phaeophyceae). Oecologia 160:483–492

    Article  Google Scholar 

  • Fukumoto LR, Mazza G (2000) Assessing antioxidant and prooxidant activities of phenolic compounds. J Agric Food Chem 48:3597–3604

    Article  CAS  Google Scholar 

  • Gómez I, Huovinen P (2010) Induction of phlorotannins during UV exposure mitigates inhibition of photosynthesis and DNA damage in the kelp Lessonia nigrescens. Photochem Photobiol 86:1056–1063

    Article  Google Scholar 

  • Gómez I, Figueroa FL, Sousa-Pinto I, Viñegla B, Pérez-Rodríguez E, Maestre C, Coelho S, Felga A, Pereira R (2001) Effects of UV radiation and temperature on photosynthesis as measured by PAM fluorescence in the red alga Gelidium pulchellum (Turner) Kützing. Bot Mar 44:9–16

    Article  Google Scholar 

  • Gómez I, Wulff A, Roleda MY, Huovinen P, Karsten U, Quartino ML, Dunton K, Wiencke C (2009) Light and temperature demands of marine benthic microalgae and seaweeds in polar regions. Bot Mar 52:593–608

  • Hanelt D (1998) Capability of dynamic photoinhibition in Arctic macroalgae is related to their depth distribution. Mar Biol 131:361–369

    Article  Google Scholar 

  • Hanelt D, Melchersmann B, Wiencke C, Nultsch W (1997) Effects of high light stress on photosynthesis of polar macroalgae in relation to depth distribution. Mar Ecol Prog Ser 149:255–266

    Article  CAS  Google Scholar 

  • Hanelt D, Tüg H, Bischof K, Groß C, Lippert H, Sawall T, Wiencke C (2001) Light regime in an Arctic fjord: a study related to stratospheric ozone depletion as a basis for determination of UV effects on algal growth. Mar Biol 138:649–658

    Article  CAS  Google Scholar 

  • Heinrich S, Valentin K, Frickenhaus S, John U, Wiencke C (2012) Transcriptomic analysis of acclimation to temperature and light stress in Saccharina latissima (Phaeophyceae). PLoS ONE 7:e44342

    Article  CAS  Google Scholar 

  • Heinrich S, Valentin K, Frickenhaus S, Wiencke C (2015) Temperature and light interactively modulate gene expression in Saccharina latissima (Phaeophyceae). J Phycol 51:93–108

    Article  CAS  Google Scholar 

  • Hoyer K, Karsten U, Sawall T, Wiencke C (2001) Photoprotective substances in Antarctic macroalgae and their variation with respect to depth distribution, different tissues and developmental stages. Mar Ecol Prog Ser 211:117–129

    Article  CAS  Google Scholar 

  • Hoyer K, Karsten U, Wiencke C (2002) Induction of sunscreen compounds in Antarctic macroalgae by different radiation conditions. Mar Biol 141:619–627

    Article  CAS  Google Scholar 

  • Huovinen P, Gómez I (2013) Photosynthetic characteristics and UV stress tolerance of Antarctic seaweeds along the depth gradient. Polar Biol 36:1319–1332

    Article  Google Scholar 

  • Iken K, Amsler CD, Hubbard JM, McClintock JB, Baker BJ (2007) Allocation patterns of phlorotannins in Antarctic brown algae. Phycologia 46:386–395

    Article  Google Scholar 

  • Karentz D, McEuen FS, Land MC, Dunlap WC (1991) Survey of mycosporine-like amino acid compounds in Antarctic marine organisms: Potential protection from ultraviolet exposure. Mar Biol 108:157–166

    Article  CAS  Google Scholar 

  • Karsten U, Wulff A, Roleda M, Müller R, Steinhoff FS, Fredersdorf J, Wiencke C (2009) Physiological responses of polar benthic micro- and macroalgae to ultraviolet radiation. Bot Mar 52:639–654

  • Koivikko R, Loponen J, Honkanen T, Jormalainen V (2005) Contents of cytoplasmic, cell-wall-bound and exudes phlorotannins in the brown alga Fucus vesiculosus, with implications on their ecological functions. J Chem Ecol 31:195–209

    Article  CAS  Google Scholar 

  • Meredith MP, King JC (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Lett 32:L19604

    Article  Google Scholar 

  • Müller R, Bartsch I, Laepple T, Wiencke C (2009) Impact of oceanic warming on the distribution of seaweeds in polar and cold-temperate waters. Bot Mar 52:617–638

  • Parages ML, Heinrich S, Wiencke C, Jiménez C (2013) Rapid phosphorylation of MAP kinase-like proteins in two species of Arctic kelps in response to temperature and UV radiation stress. Environ Exp Bot 91:30–37

    Article  CAS  Google Scholar 

  • Pavia H, Cervin G, Lindgren A, Aaberg P (1997) Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar Ecol Prog Ser 157:139–146

    Article  CAS  Google Scholar 

  • Quartino ML, Klöser H, Schloss IR, Wiencke C (2001) Biomass and associations of benthic marine macroalgae from the inner Potter Cove (King George Island, Antarctica) related to depth and substrate. Polar Biol 24:349–355

    Article  Google Scholar 

  • Rautenberger R, Bischof K (2006) Impact of temperature on UV-susceptibility of two Ulva (Chlorophyta) species from Antarctic and Subantarctic regions. Polar Biol 29:988–996

    Article  Google Scholar 

  • Rautenberger R, Bischof K (2008) UV-susceptibility of photosynthesis of adult sporophytes of four brown Antarctic macroalgae (Phaeophyceae). In: Wiencke C, Ferreyra G, Abele D, Marenssi S (eds) The Antarctic ecosystem of Potter Cove, King George Island (Isla 25 de Mayo). Synopsis of research performed 1999–2006 at the Dallmann Laboratory and Jubany Station. Rep Polar Mar Res 571, pp 263–269

  • Rautenberger R, Wiencke C, Bischof K (2013) Acclimation to UV radiation and antioxidative defence in the endemic Antarctic brown macroalga Desmarestia anceps along a depth gradient. Polar Biol 36:1779–1789

    Article  Google Scholar 

  • Richter A, Wuttke S, Zacher K (2008) Two year of in situ UV measurements at Dallmann Laboratory/Jubany Station. In: Wiencke C, Ferreyra G, Abele D, Marenssi S (eds) The Antarctic ecosystem of Potter Cove, King George Island (Isla 25 de Mayo). Synopsis of research performed 1999–2006 at the Dallmann Laboratory and Jubany Station. Rep Polar Mar Res 571, pp 12–19

  • Schloss IR, Abele D, Moreau S, Demers S, Bers AV, González O, Ferreyra GA (2012) Response of phytoplankton dynamics to 19-year (1991–2009) climate trends in Potter Cove (Antarctica). J Mar Syst 92:53–66

    Article  Google Scholar 

  • Schoenrock KM, Schram JB, Amsler CD, McClintock JB, Angus RA (2015) Climate change impacts on overstory Desmarestia spp. from the western Antarctic Peninsula. Mar Biol 162:377–389

    Article  Google Scholar 

  • Schoenwaelder MEA (2002) The occurrence and cellular significance of physodes in brown algae. Phycologia 41:125–139

    Article  Google Scholar 

  • Schreiber U, Bilger W, Neubauer C (1995) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis. Ecol Stud 100, Springer, Berlin, pp 49–70

  • Steinhoff FS, Wiencke C, Wuttke S, Bischof K (2011) Effects of water temperatures, UV radiation and low vs high PAR on phlorotannin content and germination in zoospores of Saccorhiza dermatodea (Tilopteridales, Phaeophyceae). Phycologia 50:256–263

    Article  Google Scholar 

  • Swanson AK, Druehl LD (2002) Induction, exudation and the UV protective role of kelp phlorotannins. Aquat Bot 73:241–253

    Article  CAS  Google Scholar 

  • Van de Poll WH, Eggert A, Buma AGJ, Breeman AM (2002) Temperature dependence of UV radiation effects in Arctic and temperate isolates of three red macrophytes. Eur J Phycol 37:59–68

    Article  Google Scholar 

  • Wiencke C, tom Dieck I (1989) Temperature requirements for growth and temperature tolerance of macroalgae endemic to the Antarctic region. Mar Ecol Prog Ser 54:189–197

    Article  Google Scholar 

  • Wiencke C, Rahmel J, Karsten U, Weykam G, Kirst GO (1993) Photosynthesis of marine macroalgae from Antarctica: light and temperature requirements. Bot Acta 106:78–87

    Article  Google Scholar 

  • Zacher K, Rautenberger R, Hanelt D, Wulff A, Wiencke C (2009a) The abiotic environment of polar marine benthic algae. Bot Mar 52:483–490

  • Zacher K, Roleda MY, Wulff A, Hanelt D, Wiencke C (2009b) Responses of Antarctic Iridaea cordata (Rhodophyta) tetraspores exposed to ultraviolet radiation. Phycol Res 57:186–193

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to the Comisión Nacional de Investigación Científica y Tecnológica (CONICYT-PIA), Chile, for the financial support (Projecto Anillo ART1101) of our studies. Furthermore, we thank the Instituto Antártico Chileno (INACH) for the logistical support and the opportunity to work in the laboratories at the scientific station ‘Base Profesor Julio Escudero’. We also thank the scientific diving team of Ignacio Garrido, María José Díaz, and Jorge Holtheuer for collecting the macroalgal material. This is Publication No. 2 of the grant ‘Anillo ART1101’.

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The authors have declared that no competing interests exist.

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Correspondence to Ralf Rautenberger.

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Communicated by F. Weinberger.

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Rautenberger, R., Huovinen, P. & Gómez, I. Effects of increased seawater temperature on UV tolerance of Antarctic marine macroalgae. Mar Biol 162, 1087–1097 (2015). https://doi.org/10.1007/s00227-015-2651-7

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