Advertisement

Polar Biology

, Volume 36, Issue 12, pp 1779–1789 | Cite as

Acclimation to UV radiation and antioxidative defence in the endemic Antarctic brown macroalga Desmarestia anceps along a depth gradient

  • Ralf RautenbergerEmail author
  • Christian Wiencke
  • Kai Bischof
Original Paper

Abstract

The endemic Antarctic brown macroalga Desmarestia anceps colonizes the subtidal between 5 and 30 m in Potter Cove on King George Island (South Shetland Islands, Antarctica). Experiments were conducted to study photosynthetic activities, antioxidative enzymes and UV tolerance of field-grown individuals with respect to the light histories along different subtidal positions. Individuals collected from the upper (5.5 m) and mid-subtidal (9.0 m) are characterized by high maximum electron transport rates (ETRmax) measured by PAM-fluorometry and high activities of superoxide dismutase (SOD) supported by considerable activities of glutathione reductase. Individuals of this species from the upper subtidal are able to tolerate high irradiances of UV-B radiation because its photosynthetic apparatus is putatively well protected by phlorotannins. In contrast, individuals from lower subtidal positions (13.5 and 15.5 m) showed an opposite trend: lower ETRmax and SOD activities as well as a lower UV tolerance of photosynthesis. Moreover, a non-denaturing polyacrylamide gel electrophoresis (native PAGE) of a partially purified crude extract reveals that D. anceps has probably six isoforms of SOD. These intra-specific patterns imply a high phenotypical plasticity of D. anceps with respect to its photosynthesis and photoprotective mechanisms. Overall, photosynthesis, UV tolerance and antioxidative potential are highly regulated in D. anceps corresponding to the respective light regimes along its natural growth sites.

Keywords

Desmarestia anceps Superoxide dismutase Antarctica Photosynthesis UV radiation Oxidative stress 

Notes

Acknowledgments

The authors thank the Alfred Wegener Institute for Polar and Marine Research (AWI) in Bremerhaven and the Dirección Nacional del Antártico (DNA) in Buenos Aires for financial and logistical support to work in the Dallmann Laboratory at Carlini Station. Funding was also provided by both the “Deutsche Forschungsgemeinschaft” (BI 772/2-1,2) and the “Helmholtz-Gemeinschaft deutscher Forschungszentren” (VH-NG-059). Our studies would not have been possible without the efficient support by the scientific diving team at Carlini Station in January 2005 (Ulrich and Jana Barenbrock, Katharina Zacher). Technical assistance in the laboratory by Alice Schneider and Meri Eichner is also gratefully acknowledged.

References

  1. Aguilera J, Rautenberger R (2011) Oxidative stress tolerance strategies of intertidal macroalgae. In: Abele D, Vázquez-Medina JP, Zenteno-Savín T (eds) Oxidative Stress in Aquatic Ecosystems. Wiley-Blackwell, Hokoken, pp 58–71CrossRefGoogle Scholar
  2. Aguilera J, Dummermuth A, Karsten U, Schriek R, Wiencke C (2002a) Enzymatic defences against photooxidative stress induced by ultraviolet radiation in Arctic marine macroalgae. Mar Biol 140:1087–1095Google Scholar
  3. Aguilera J, Bischof K, Karsten U, Hanelt D, Wiencke C (2002b) Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. II. Pigment accumulation and biochemical defence systems against high light stress. Mar Biol 140:1087–1095CrossRefGoogle Scholar
  4. Aro EM, Virgin I, Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134PubMedCrossRefGoogle Scholar
  5. Asada K (2000) The water–water cycle as alternative photon and electron sinks. Philos Trans R Soc Lond B 355:1419–1431CrossRefGoogle Scholar
  6. Becker S, Graeve M, Bischof K (2010) Photosynthesis and lipid composition in the Antarctic rhodophyte Palmaria decipiens: effects of changing light and temperature levels. Polar Biol 33:945–955CrossRefGoogle Scholar
  7. Bilger W, Veit M, Schreiber L, Schreiber U (1997) Measurement of leaf epidermal transmittance of UV radiation by chlorophyll fluorescence. Physiol Plant 101:754–763CrossRefGoogle Scholar
  8. Bischof K, Rautenberger R (2012) Seaweed responses to environmental stress: reactive oxygen and antioxidative strategies. In: Wiencke C, Bischof K (eds) Seaweed biology. Novel insights into ecophysiology, ecology and utilization. Ecological Studies 219, Springer, Heidelberg, pp 109–132Google Scholar
  9. Bischof K, Hanelt D, Wiencke C (1998a) UV-radiation can affect depth-zonation of Antarctic macroalgae. Mar Biol 131:597–605CrossRefGoogle Scholar
  10. Bischof K, Hanelt D, Tüg H, Karsten U, Brouwer PEM, Wiencke C (1998b) Acclimation of brown algal photosynthesis to ultraviolet radiation in Arctic coastal waters (Spitsbergen, Norway). Polar Biol 20:388–395CrossRefGoogle Scholar
  11. Bischof K, Hanelt D, Wiencke C (2000) Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae. Planta 211:555–562PubMedCrossRefGoogle Scholar
  12. Bischof K, Hanelt D, Aguilera J, Karsten U, Vögele B, Sawall T, Wiencke C (2002) Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. I. Sensitivity of photosynthesis to ultraviolet radiation. Mar Biol 140:1097–1106CrossRefGoogle Scholar
  13. Bischof K, Gomez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda MY, Zacher K, Wiencke C (2006a) Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Biotechnol 5:141–166CrossRefGoogle Scholar
  14. Bischof K, Rautenberger R, Brey L, Pérez-Lloréns JL (2006b) Physiological acclimation to gradients of solar irradiance within mats of the filamentous green macroalga Chaetomorpha linum from southern Spain. Mar Ecol Prog Ser 306:165–175CrossRefGoogle Scholar
  15. Bouchard JN, Roy S, Campbell DA (2006) UVB Effects on the photosystem II D1 protein of phytoplankton and natural phytoplankton communities. Photochem Photobiol 82:936–951PubMedCrossRefGoogle Scholar
  16. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  17. Caldwell MM (1971) Solar UV radiation and the growth and development of higher plants. In: Giese AC (ed) Photophysiology. Current topics in photobiology and photochemistry 6, Academic Press, New York, pp 131–177Google Scholar
  18. Chen CN, Pan SM (1996) Assay of superoxide dismutase activity by combining electrophoresis and densitometry. Bot Bull Acad Sinica 37:107–111Google Scholar
  19. Cock JM, Sterck L, Rouze P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury J-M, Badger JH, Beszteri B, Billiau K, Bonnet E, Bothwell JH, Bowler C, Boyen C, Brownlee C, Carrano CJ, Charrier B, Cho GY, Coelho SM, Collen J, Corre E, Da Silva C, Delage L, Delaroque N, Dittami SM, Doulbeau S, Elias M, Farnham G, Gachon CMM, Gschloessl B, Heesch S, Jabbari K, Jubin C, Kawai H, Kimura K, Kloareg B, Kupper FC, Lang D, Le Bail A, Leblanc C, Lerouge P, Lohr M, Lopez PJ, Martens C, Maumus F, Michel G, Miranda-Saavedra D, Morales J, Moreau H, Motomura T, Nagasato C, Napoli CA, Nelson DR, Nyvall-Collen P, Peters AF, Pommier C, Potin P, Poulain J, Quesneville H, Read B, Rensing SA, Ritter A, Rousvoal S, Samanta M, Samson G, Schroeder DC, Segurens B, Strittmatter M, Tonon T, Tregear JW, Valentin K, von Dassow P, Yamagishi T, Van de Peer Y, Wincker P (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–621Google Scholar
  20. Collén J, Davison IR (1999) Stress tolerance and reactive oxygen metabolism in the intertidal red seaweeds Mastocarpus stellatus and Chondrus crispus. Plant Cell Environ 22:1143–1151CrossRefGoogle Scholar
  21. Collén J, Porcel B, Carré W, Ball SG, Chaparro C, Tonon T, Barbeyron T, Michel G, Noel B, Valentin K, Elias M, Artiguenave F, Arun A, Aury J-M, Barbosa-Neto JF, Bothwell JH, Bouget F-Y, Brillet L, Cabello-Hurtado F, Capella-Gutiérrez S, Charrier B, Cladière L, Cock JM, Coelho SM, Colleoni C, Czjzek M, Da Silva C, Delage L, Denoeud F, Deschamps P, Dittami SM, Gabaldón T, Gachon CMM, Groisillier A, Hervé C, Jabbari K, Katinka M, Kloareg B, Kowalczyk N, Labadie K, Leblanc C, Lopez PJ, McLachlan DH, Meslet-Cladiere L, Moustafa A, Nehr Z, Nyvall Collén P, Panaud O, Partensky F, Poulain J, Rensing SA, Rousvoal S, Samson G, Symeonidi A, Weissenbach J, Zambounis A, Wincker P, Boyen C (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci USA 110:5247–5252Google Scholar
  22. 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 88:58–66PubMedCrossRefGoogle Scholar
  23. 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 160:1–13CrossRefGoogle Scholar
  24. de Jesus MD, Tabatabai F, Chapman DJ (1989) Taxonomic distribution of copper-zinc superoxide dismutase in green algae and its phylogenetic importance. J Phycol 25:767–772CrossRefGoogle Scholar
  25. Dring MJ (2005) Stress Resistance and Disease Resistance in Seaweeds: the Role of Reactive Oxygen Metabolism. In: Callow JA (ed) Adv Bot Res 43:175–207Google Scholar
  26. 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 28:680–686CrossRefGoogle Scholar
  27. Goldberg DM, Spooner RJ (1983) Glutathione reductase. In: Bergmeyer HU (ed) Enzymes. 1. Oxidoreductases, transferases, VCH, Weinheim, pp 258–265Google Scholar
  28. 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 86:1056–1063PubMedCrossRefGoogle Scholar
  29. Gómez I, Weykam G, Klöser H, Wiencke C (1997) Photosynthetic light requirements, metabolic carbon balance and zonation of sublittoral macroalgae from King George Island (Antarctica). Mar Ecol Prog Ser 148:281–293CrossRefGoogle Scholar
  30. 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 52:593–608CrossRefGoogle Scholar
  31. Hanelt D (1996) Photoinhibition of photosynthesis in marine macroalgae. Sci Mar 60:243–248Google Scholar
  32. Hanelt D (1998) Capability of dynamic photoinhibition in Arctic macroalgae is related to their depth distribution. Mar Biol 131:361–369CrossRefGoogle Scholar
  33. Hanelt D, Jaramillo MJ, Nultsch W, Senger S, Westermeier R (1994) Photoinhibition as a regulative mechanism of photosynthesis in marine algae of Antarctica. Ser Cient Inst Antart Chile 44:67–77Google Scholar
  34. Hanelt D, Melchersmann B, Wiencke C, Nultsch W (1997a) Effects of high light stress on photosynthesis of polar macroalgae in relation to depth distribution. Mar Ecol Prog Ser 149:255–266CrossRefGoogle Scholar
  35. Hanelt D, Wiencke C, Karsten U, Nultsch W (1997b) Photoinhibition and recovery after high light stress in different developmental and life-history stages of Laminaria saccharina (Phaeophyta). J Phycol 33:387–395CrossRefGoogle Scholar
  36. 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 138:649–658CrossRefGoogle Scholar
  37. 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:e44342PubMedCrossRefGoogle Scholar
  38. Iken K (1996) Trophic relations between macroalgae and herbivores in Potter Cove (King Georg Island, Antarctica). Rep Polar Res 201:206Google Scholar
  39. Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547CrossRefGoogle Scholar
  40. Johansson G, Snoeijs P (2002) Macroalgal photosynthetic responses to light in relation to thallus morphology and depth zonation. Mar Ecol Prog Ser 244:63–72CrossRefGoogle Scholar
  41. 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 52:639–654CrossRefGoogle Scholar
  42. Klöser H, Arntz WE (1994) Research on Antarctic shallow coastal and littoral systems. Polarforschung 64:27–41Google Scholar
  43. Klöser H, Quartino ML, Wiencke C (1996) Distribution of macroalgae and macroalgal communities in gradients of physical conditions in Potter Cove, King George Island, Antarctica. Hydrobiologia 333:1–17CrossRefGoogle Scholar
  44. McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymatic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055PubMedGoogle Scholar
  45. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefGoogle Scholar
  46. Moe RL, Silva PC (1977) Antarctic marine flora: uniquely devoid of kelps. Science 196:1206–1208PubMedCrossRefGoogle Scholar
  47. Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92PubMedCrossRefGoogle Scholar
  48. 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 91:30–37CrossRefGoogle Scholar
  49. 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 157:139–146CrossRefGoogle Scholar
  50. Pescheck F, Bischof K, Bilger W (2010) Screening of UV-A and UV-B radiation in marine green macroalgae (Chlorophyta). J Phycol 46:444–455CrossRefGoogle Scholar
  51. Poulson ME, McNeil AJ, Donahue RA (2011) Photosynthetic response of Nereocystis luetkeana (Phaeophyta) to high light. Phycol Res 59:156–165CrossRefGoogle Scholar
  52. Quartino ML, Boraso de Zaixso A (2008) Summer macroalgal biomass in Potter Cove, South Shetland Islands, Antarctica: its production and flux to the ecosystem. Polar Biol 31:281–294CrossRefGoogle Scholar
  53. 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 24:349–355CrossRefGoogle Scholar
  54. Rautenberger R, Bischof K (2006) Impact of temperature on UV-susceptibility of two Ulva (Chlorophyta) species from Antarctic and Subantarctic regions. Polar Biol 29:988–996CrossRefGoogle Scholar
  55. 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 Google Scholar
  56. Rautenberger R, Mansilla A, Gómez I, Wiencke C, Bischof K (2009) Photosynthetic responses to UV-radiation of intertidal macroalgae from the Strait of Magellan (Chile). Rev Chil Hist Nat 82:43–61CrossRefGoogle Scholar
  57. 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 Res 571, pp 12–19Google Scholar
  58. Rodrigues MA, dos Santos CP, Young AJ, Strbac D, Hall DO (2002) A smaller and impaired xanthophyll cycle makes the deep sea macroalgae Laminaria abyssalis (Phaeophyceae) highly sensitive to daylight when compared with shallow water Laminaria digitata. J Phycol 38:939–947CrossRefGoogle Scholar
  59. Runcie JW, Riddle MJ (2006) Photosynthesis of marine macroalgae in ice-covered and ice-free environments in East Antarctica. Eur J Phycol 41:223–233CrossRefGoogle Scholar
  60. Runcie JW, Riddle MJ (2011) Distinguishing downregulation from other non-photochemical quenching of an Antarctic benthic macroalga using in situ fluorometry. Eur J Phycol 46:171–180CrossRefGoogle Scholar
  61. Sagert S, Forster RM, Feuerpfeil P, Schubert H (1997) Daily course of photosynthesis and photoinhibition in Chondrus crispus (Rhodophyta) from different shore levels. Eur J Phycol 32:363–371Google Scholar
  62. Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis. Ecological Studies 100, Springer, Heidelberg, pp 49–70Google Scholar
  63. Schriek R (2000) Effects of light and temperature on the enzymatic antioxidative defense systems in the Antarctic ice diatom Entomoneis kufferathii Manguin. Ber Polarforsch Meeresforsch 349:1–130Google Scholar
  64. Udilova N (1999) Vergleichende Untersuchungen von Methoden zum Nachweis von Superoxidradikalen in biologischen und Modellsystemen. Doctoral thesis. Humboldt University of Berlin (in German)Google Scholar
  65. Vieira Dos Santos C, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11:329–334PubMedCrossRefGoogle Scholar
  66. Waring J, Klenell M, Bechtold U, Underwood GJC, Baker NR (2010) Light-induced responses of oxygen photoreduction, reactive oxygen species production and scavenging in two diatom species. J Phycol 46:1206–1217CrossRefGoogle Scholar
  67. Weykam G, Gomez I, Wiencke C, Iken K, Klöser H (1996) Photosynthetic characteristics and C:N ratios of macroalgae from King George Island (Antarctica). J Exp Mar Biol Ecol 204:1–22CrossRefGoogle Scholar
  68. Wiencke C, Fischer G (1990) Growth and stable carbon isotope composition of cold-water macroalgae in relation to light and temperature. Mar Ecol Prog Ser 65:283–292CrossRefGoogle Scholar
  69. Wu T-M, Hsu Y-T, Sung M-S, Hsu Y-T, Lee T-M (2009a) Expression of genes involved in redox homeostasis and antioxidant defense in a marine macroalga Ulva fasciata by excess copper. Aquat Toxicol 94:275–285PubMedCrossRefGoogle Scholar
  70. Wu T-M, Hsu Y-T, Lee T-M (2009b) Effects of cadmium on the regulation of antioxidant enzyme activity, gene expression, and antioxidant defenses in the marine macroalga Ulva fasciata. Bot Stud 50:25–34Google Scholar
  71. Wulff A, Iken K, Quartino ML, Al-Handal A, Wiencke C, Clayton MN (2009) Biodiversity, biogeography and zonation of marine benthic micro- and macroalgae in the Arctic and Antarctic. Bot Mar 52:491–507CrossRefGoogle Scholar
  72. Xiong F (2001) Evidence that UV-B tolerance of the photosynthetic apparatus in microalgae is related to the D1-turnover mediated repair cycle in vivo. J Plant Physiol 158:285–294CrossRefGoogle Scholar
  73. Zacher K, Roleda MY, Hanelt D, Wiencke C (2006) UV effects on photosynthesis and DNA in propagules of three Antarctic seaweeds (Adenocystis utricularis, Monostroma hariotii and Porphyra endiviifolium). Planta 225:1505–1516PubMedCrossRefGoogle Scholar
  74. Zacher K, Rautenberger R, Hanelt D, Wulff A, Wiencke C (2009) The abiotic environment of polar marine benthic algae. Bot Mar 52:483–490CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Ralf Rautenberger
    • 1
    • 2
    Email author
  • Christian Wiencke
    • 3
  • Kai Bischof
    • 4
  1. 1.Institute for Polar EcologyChristian Albrechts University of KielKielGermany
  2. 2.Department of BotanyUniversity of OtagoDunedinNew Zealand
  3. 3.Department Seaweed Biology, Section Functional EcologyAlfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany
  4. 4.Department of Marine Botany, Faculty of Biology and ChemistryUniversity of BremenBremenGermany

Personalised recommendations