Journal of Applied Phycology

, Volume 30, Issue 2, pp 1247–1257 | Cite as

Phenolics as photoprotective mechanism against combined action of UV radiation and temperature in the red alga Gracilaria chilensis?

  • Edgardo Cruces
  • María Rosa Flores-Molina
  • María José Díaz
  • Pirjo Huovinen
  • Iván Gómez


The rhodophyte Gracilaria chilensis is a structuring species of the estuarine and fjord systems in southern Chile and is commercially exploited from natural and farmed populations. Due to its capacity to tolerate extreme variations in environmental conditions, this species is an excellent model organism to examine stress tolerance mechanisms. The present study examined the combined effect of temperature and UV radiation on the reproductive phases of G. chilensis (carposporophyte, tetrasporophyte, and vegetative) at the lower and upper intertidals of the Valdivia River estuary. The concentration of phenolic compounds and their antioxidant capacity as well as the inhibition of primary photochemical reactions, measured as the fluorescence of photosystem II, was determined. The kinetics of the maximal quantum yield (F v/F m) between 5 and 50 °C indicated a rapid decrease of photosynthesis from 35 °C upwards in the three reproductive phases. Exposures for 1, 6, 24, and 48 h to photosythetically active radiation (PAR) and PAR + UV at 5, 25, and 35 °C affected photosynthesis in the three reproductive phases, especially at the elevated temperature of 35 °C where the maximum cumulative decreases of F v/F m were close to 93 and 98% in tetrasporophytes and carposporophytes. An important finding was the high content of phenols, which increased with increasing UV doses only at 10 °C, especially in carposporophytic and vegetative thalli. The antioxidant activity increased at 10 and 25 °C in algae exposed to UV radiation, while at low (5 °C) and elevated (35 °C) temperatures, it resulted in the inhibition of antioxidant activity. Overall, phenols were positively correlated with the antioxidant activity and F v/F m, especially in tetrasporophytes. The study revealed that the different life history phases of G. chilensis showed similar stress tolerance mechanisms, which appeared to be triggered strongly by temperature and less by UV radiation.


Gracilaria chilensis Rhodophyta Estuary Photosynthesis, phenolics, temperature UV radiation 



The helpful technical assistance of J. Holtheuer is acknowledged.

Funding information

This study was supported by the FONDECYT grant nos. 1130794 and 1161129, the FONDAP-IDEAL no. 15150003 to I.G. and P.H., and the FONDECYT grant no. 3130516 to E.C.


  1. Abreu MH, Pereira R, Sousa-Pinto I, Yarish C (2011) Ecophysiological studies of the non-indigenous species Gracilaria vermiculophylla (Rhodophyta) and its abundance patterns in Ria de Aveiro lagoon, Portugal. Eur J Phycol 46:453–464CrossRefGoogle Scholar
  2. Athukorala Y, Lee K-W, Song C, Ahn C-B, Shin T-S, Cha Y-J, Shahidi F, Jeon Y-J (2003) Potential antioxidant activity of marine red alga Grateloupia filicina extracts. J Food Lipids 10:251–265CrossRefGoogle Scholar
  3. Ayres-Ostrock L, Plastino E (2014) Effects of short-term exposure to ultraviolet-B radiation on photosynthesis and pigment content of red (wild types), greenish-brown, and green strains of Gracilaria birdiae (Gracilariales, Rhodophyta). J Appl Phycol 26:867–879CrossRefGoogle Scholar
  4. Bird C, McLachlan J, Oliveira E (1986) Gracilaria chilensis sp. nov. (Rhodophyta, Gigartinales), from Pacific South America. Can J Bot 64:2928–2934CrossRefGoogle Scholar
  5. Bischof K, Kräbs G, Wiencke C, Hanelt D (2002) Solar ultraviolet radiation affects the activity of ribulose-1, 5-bisphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L. Planta 215:502–509CrossRefPubMedGoogle Scholar
  6. Bischof K, Rautenberger R (2012) Seaweeds responses to environmental stress: reactive oxygen and antioxidative strategies. In: Wiencke C, Bischof K (eds) Seaweed biology—novel insights into ecophysiology, ecology and utilization. Springer, Berlin, pp 109–132Google Scholar
  7. Bonomi-Barufi J, Korbee N, Oliveira M, Figueroa FL (2011) Effects of N supply on the accumulation of photosynthetic pigments and photoprotectors in Gracilaria tenuistipitata (Rhodophyta) cultured under N limitation. J Appl Phycol 23:457–466CrossRefGoogle Scholar
  8. Brand-Williams W, Cuvelier M, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 28:25–30CrossRefGoogle Scholar
  9. Brown L, McLachlan J (1982) Atypical carotenoids for Rhodophyceae in the genus Gracilaria (Gigartinales). Phycologia 21:9–16CrossRefGoogle Scholar
  10. Buchner O, Holzinger A, Luetz C (2007) Effects of temperature and light on the formation of chloroplast protrusions in leaf mesophyll cells of high alpine plants. Plant Cell Environ 30:1347–1356CrossRefPubMedGoogle Scholar
  11. Buschmann AH, Westermeier R, Retamales C (1995) Cultivation of Gracilaria in the sea-bottom in southern Chile: a review. J Appl Phycol 7:291–301CrossRefGoogle Scholar
  12. Buschmann AH, Varela DA, Hernández-González C, Huovinen P (2008) Opportunities and challenges for the development of an integrated seaweed-based aquaculture activity in Chile: determining the physiological capabilities of Macrocystis and Gracilaria as biofilters. J Appl Phycol 20:571–577CrossRefGoogle Scholar
  13. Candia A (1991) The life-history of Gracilaria (Rhodophyta, Gracilariales)—deviations in the reproductive pattern and genetic-implications. Rev Chil Hist Nat 64:331–334Google Scholar
  14. Carmona R, Santos R (2006) Is there an ecophysiological explanation for the gametophyte–tetrasporophyte ratio in Gelidium sesquipedale (Rhodophyta)? J Phycol 42:259–269CrossRefGoogle Scholar
  15. Collén J, Davidson 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
  16. Connan S, Delisle F, Deslandes E, Ar Gall E (2006) Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Bot Mar 49:39–46CrossRefGoogle Scholar
  17. 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 88:58–66CrossRefPubMedGoogle Scholar
  18. 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
  19. Cruces E, Rojas-Lillo Y, Ramírez-Kushel E, Atala E, López-Alarcón C, Lissi E, Gómez I (2016) Comparison of different techniques for the preservation and extraction of phlorotannins in the kelp Lessonia spicata (Phaeophyceae): assays of DPPH, ORAC-PGR and ORAC-FL as testing methods. J Appl Phycol 28:573–580CrossRefGoogle Scholar
  20. Destombe C, Godin J, Lefebvre C, Dehorter O, Vernet P (1992) Differences in dispersal abilities of haploid and diploid spores of Gracilaria verrucosa (Gracilariales, Rhodophyta). Bot Mar 35:93–98CrossRefGoogle Scholar
  21. Edding M, León C, Tala F (2006) Morphological variations of Gracilaria chilensis Bird, McLachlan, Oliveira, 1968 (Rhodophyta, Gracilariales) in the Southeast Pacific. Gayana 70:220–227Google Scholar
  22. Engel C, ÅBerg P, Gaggiotti OE, Destombe C, Valero M (2001) Population dynamics and stage structure in a haploid-diploid red seaweed, Gracilaria gracilis. J Ecol 89:436–450CrossRefGoogle Scholar
  23. Flores-Molina MR, Rautenberger R, Muñoz P, Huovinen P, Gómez I (2016) Stress tolerance of the endemic Antarctic brown alga to UV radiation and temperature is mediated by high concentrations of phlorotannins. Photochem Photobiol 92:455–466Google Scholar
  24. Franklin LA, Forster RM (1997) Review the changing irradiance environment: consequences for marine macrophyte physiology, productivity and ecology. Eur J Phycol 32:207–232Google Scholar
  25. Gao K, Xu J (2008) Effects of solar UV radiation on diurnal photosynthetic performance and growth of Gracilaria lemaneiformis (Rhodophyta). Eur J Phycol 43:297–307CrossRefGoogle Scholar
  26. Garcés-Vargas J, Ruiz M, Pardo LM, Nuñez S, Pérez-Santos I (2013) Caracterización hidrográfica del estuario del río Valdivia, centro-sur de Chile. Lat Am J Aquat Res 41:113–125CrossRefGoogle Scholar
  27. Goiris K, Muylaert K, Fraeye I, Foubert I, De Brabanter J, De Cooman L (2012) Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. J Appl Phycol 24:1477–1486CrossRefGoogle Scholar
  28. Gómez I, Figueroa FL, Huovinen P, Ulloa N, Morales V (2005) Photosynthesis of the red alga Gracilaria chilensis under natural solar radiation in an estuary in southern Chile. Aquaculture 244:369–382CrossRefGoogle Scholar
  29. 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 86:1056–1063CrossRefPubMedGoogle Scholar
  30. Gómez I, Orostegui M, Huovinen P (2007) Morpho-functional patterns of photosynthesis in the South Pacific kelp Lessonia nigrescens: effects of UV radiation on 14C fixation and primary photochemical reactions. J Phycol 43:55–64CrossRefGoogle Scholar
  31. Grzymski J, Johnsen G, Sakshaug E (1997) The significance of intracellular selfshading on the bio optical properties of brown, red and green macroalgae. J Phycol 33:408–414CrossRefGoogle Scholar
  32. Guillemin M-L, Sepúlveda RD, Correa JA, Destombe C (2013) Differential ecological responses to environmental stress in the life history phases of the isomorphic red alga Gracilaria chilensis (Rhodophyta). J Appl Phycol 25:215–224CrossRefGoogle Scholar
  33. Hagerman AE, Riedl KM, Jones AG, Sovik KN, Ritchard NT, Hartzfeld PW, Riechel TL (1998) High molecular weight plant polyphenolics (tannins) as biological antioxidants. J Agric Food Chem 46:1887–1892CrossRefPubMedGoogle Scholar
  34. Hoffmann JR, Hansen LJ, Klinger T (2003) Interactions between UV radiation and temperature limit interferences from single-factor experiments. J Phycol 39:268–272CrossRefGoogle Scholar
  35. 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 211:117–129CrossRefGoogle Scholar
  36. Huovinen P, Gómez I (2011) Spectral attenuation of solar radiation in Patagonian fjord and coastal waters and implications for algal photobiology. Cont Shelf Res 31:254–259CrossRefGoogle Scholar
  37. Huovinen P, Gómez I, Figueroa FL, Ulloa N, Morales V, Lovengreen C (2004) Ultraviolet-absorbing mycosporine-like amino acids in red macroalgae from Chile. Bot Mar 47:21–29CrossRefGoogle Scholar
  38. Huovinen P, Gómez I, Lovengreen C (2006) A five-year study of solar ultraviolet radiation in Southern Chile (39°S): potential impact on physiology of coastal marine algae? Photochem Photobiol 82:515–522CrossRefPubMedGoogle Scholar
  39. Jones LW, Kok B (1966) Photoinhibition of chloroplast reactions. 1 Kinetics and action spectrum. Plant Physiol 41:1037–1043CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kain JM, Destombe C (1995) A review of the life history, reproduction and phenology of Gracilaria. J Appl Phycol 7:269–281CrossRefGoogle Scholar
  41. Lapointe BE, Tenore KR, Dawes CJ (1984) Interactions between light and temperature on the physiological ecology of Gracilaria tikvahiae (Gigartinales: Rhodophyta). Mar Biol 80:161–170CrossRefGoogle Scholar
  42. Mable BK, Otto SP (1998) The evolution of life cycles with haploid and diploid phases. BioEssays 20:453–462CrossRefGoogle Scholar
  43. Marquart R, Schubert H, Varela DA, Huovinen P, Henríquez L, Buschmann AH (2010) Light acclimation strategies of three commercially important red algal species. Aquaculture 299:140–148CrossRefGoogle Scholar
  44. Pérez-Rodríguez E, Gómez I, Karsten U, Figueroa FL (1998) Effects of UV radiation on photosynthesis and excretion of UV-absorbing compounds of Dasycladus vermicularis (Dasycladales, Chlorophyta) from southern Spain. Phycologia 37:379–387CrossRefGoogle Scholar
  45. Pérez-Rodríguez E, Aguilera J, Gómez I, Figueroa FL (2001) Excretion of coumarins by the Mediterranean alga Dasycladus vermicularis in response to environmental stress. Mar Biol 139:633–639CrossRefGoogle Scholar
  46. Prieto I, Westermeier R, Müller D (1991) Variation of phenophases of Gracilaria chilensis Bird, McLaughlin and Oliveira (Rhodophyta, Gigartinales) in laboratory and field culture conditions: presence of mixed phases. Rev Chil Hist Nat 64:343–352Google Scholar
  47. Rautenberger R, Bischof K (2006) Impact of temperature on UV-susceptibility of two Ulva (Chlorophyta) species from Antarctic and Subantarctic regions. Polar Biol 29:988–996Google Scholar
  48. Roleda MY, van de Poll WH, Hanelt D, Wiencke C (2004) PAR and UVBR effects on photosynthesis, viability, growth and DNA in different life stages of two coexisting Gigartinales: implications for recruitment and zonation pattern. Mar Ecol Prog Ser 281:37–50CrossRefGoogle Scholar
  49. Roleda MY, Nyberg CD, Wulff A (2012) UVR defense mechanisms in eurytopic and invasive Gracilaria vermiculophylla (Gracilariales, Rhodophyta). Physiol Plant 146:205–216CrossRefPubMedGoogle Scholar
  50. Rostagno MA, Palma M, Barroso CG (2003) Ultrasound-assisted extraction of soy isoflavones. J Chromatogr A 1012:119–128CrossRefPubMedGoogle Scholar
  51. Schmidt ÉC, dos Santos RM, Horta PA, Maraschin M, Bouzon ZL (2010) Effects of UVB radiation on the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales): changes in cell organization, growth and photosynthetic performance. Micron 41:919–930CrossRefPubMedGoogle Scholar
  52. Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. Ecol Stud 100:49–70Google Scholar
  53. Schoenwaelder MEA (2002) The occurrence and cellular significance of physodes in brown algae. Phycologia 41:125–139CrossRefGoogle Scholar
  54. Setlov RB (1974) The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis‬‬‬‬‬‬‬‬‬‬‬‬‬‬‬‬‬‬‬‬‬‬‬‬. Proc Nat‬ Acad Sci USA 71:3363–3366CrossRefGoogle Scholar
  55. Slatkin M, Wade M (1978) Group selection on a quantitative character. Proc Natl Acad Sci 75:3531–3534CrossRefPubMedPubMedCentralGoogle Scholar
  56. Smillie RM, Critchley C, Bain JM, Nott R (1978) Effect of growth temperature on chloroplast structure and activity in barley. Plant Physiol 62:191–196CrossRefPubMedPubMedCentralGoogle Scholar
  57. Takaichi S (2011) Carotenoids in algae: distributions, biosyntheses and functions. Mar Drugs 9:1101–1118CrossRefPubMedPubMedCentralGoogle Scholar
  58. Thomsen MS, McGlathery K (2006) Effects of accumulations of sediments and drift algae on recruitment of sessile organisms associated with oyster reefs. J Exp Mar Biol Ecol 328:22–34CrossRefGoogle Scholar
  59. Ursi S, Pedersén M, Plastino E, Snoeijs P (2003) Intraspecific variation of photosynthesis, respiration and photoprotective carotenoids in Gracilaria birdiae (Gracilariales, Rhodophyta). Mar Biol 142:997–1007CrossRefGoogle Scholar
  60. Xu J, Gao K (2010) UV-A enhanced growth and UV-B induced positive effects in the recovery of photochemical yield in Gracilaria lemaneiformis (Rhodophyta). J Photochem Photobiol B 100:117–122CrossRefPubMedGoogle Scholar
  61. Yildiz G, Vatan Ö, Çelikler S, Dere Ş (2011) Determination of the phenolic compounds and antioxidative capacity in red algae Gracilaria bursa-pastoris. Int J Food Prop 14:496–502CrossRefGoogle Scholar
  62. Zheng Y (2013) Combined effects of light and nitrate supplies on the growth, photosynthesis and ultraviolet-absorbing compounds in marine macroalga Gracilaria lemaneiformis (Rhodophyta), with special reference to the effects of solar ultraviolet radiation. Phycol Res 61:89–97CrossRefGoogle Scholar
  63. Zou D, Gao K (2013) Thermal acclimation of respiration and photosynthesis in the marine macroalga Gracilaria lemaneiformis (Gracilariales, Rhodophyta). J Phycol 49:61–68CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Edgardo Cruces
    • 1
    • 2
  • María Rosa Flores-Molina
    • 1
  • María José Díaz
    • 1
    • 3
  • Pirjo Huovinen
    • 1
    • 4
  • Iván Gómez
    • 1
    • 4
  1. 1.Instituto de Ciencias Marinas y LimnológicasUniversidad Austral de ChileValdiviaChile
  2. 2.Centro Integrativo de Biología y Química Aplicada (CIBQA)Universidad Bernardo OHigginsSantiagoChile
  3. 3.Section Functional Ecology-Rocky Shore EcologyAlfred Wegener Institute Polar and Marine ResearchBremerhavenGermany
  4. 4.FONDAP Research Center Dynamic of High Latitude Marine Ecosystems (IDEAL)ValdiviaChile

Personalised recommendations