Journal of Applied Phycology

, 11:559 | Cite as

Phenolic compounds and antioxidant properties in the snow alga Chlamydomonas nivalis after exposure to UV light

  • Brian Duval
  • Kalidas Shetty
  • William H. Thomas


The snow alga Chlamydomonas nivalis was collected from the Sierra Nevada, California, USA, and examined for its ability to produce phenolic compounds, free proline, and provide antioxidant protection factor in response to UV-A and UV-C light. Exposure of C. nivalis cells to UV-A light (365nm) for 5 days resulted in a 5–12% increase in total phenolics, where as exposure to UV-C light (254 nm) resulted in a 12–24% increase in phenolics after 7 days of exposure. Free proline was not affected by UV-A, but increased markedly after UV-C exposure. A three-fold increase in free proline occurred within two days after exposure to UV-C, but then dropped as cells became bleached. Antioxidant protection factor (PF) increased after treatment of cells with UV-A and remained constant throughout UV-C exposure. Spectral analysis of algal extracts revealed a decrease in absorption in the 215–225 nm region, short-term (2day) stimulation of pigment at 280 nm, and an increase in carotenoids (473 nm), after exposure to UV-A. Snow alga exposed to UV-C light had a different spectrum from that of UV-A exposed cells, i.e. an enhancement of three major peaks at 220, 260, and 280 nm, and loss of absorption in the carotenoid region.We report that UV light exposure, especially in the UV-C range, can stimulate phenolic-antioxidant production in aplanospores of C. nivalis effecting biochemical pathways related to proline metabolism.

Chlamydomonas nivalis UV-C exposure snow alga phenolic compounds antioxidant protection proline metabolism 


  1. Alia PSP (1993) Suppression in mitochondrial electron transport is the prime cause behind stress induced proline accumulation. Biophys. Res. Commun. 193: 54–58.CrossRefGoogle Scholar
  2. Alia PSP, Mohanty P (1991) Proline enhances primary photochemical activities in isolated thylakoid membranes of Brassica juncea by arresting photoinhibitory damage. Biochem. biophys. Res. Commun. 181: 1238–1244.PubMedCrossRefGoogle Scholar
  3. Andarwulan N, Shetty K (1999) Phenolic content in differentiated tissue cultures of untransformed and Agrobacterium-transformed roots of anise (Pimpinella anisum L.). J. agric. Food Chem 47: 1776–1780.PubMedCrossRefGoogle Scholar
  4. Ballare CL, Barnes PW, Flint SD, Price S (1995) Inhibition of hypocotyl elongation by ultraviolet-B radiation in de-etiolating tomato seedlings. II. Time-course, comparison, with flavonoid responses and adaptive significance. Physiol. Plant. 93: 593–601.CrossRefGoogle Scholar
  5. Balzer I, Hardeland R (1996) Melatonin in algae and higher plantspossible new roles as a phytohormones and antioxidant. Botanica Acuta 109: 180–183.Google Scholar
  6. Bidigare RR, Ondrusek ME, Kennicutt MC, Iturriaga R, Harvey HR, Hoham RW, Macko SA (1993) Evidence for a protective function for secondary catotenoids of snow algae. J. Phycol. 29: 427–434.CrossRefGoogle Scholar
  7. Blunden G (1993) Marine algae as sources of biologically active compounds. Interdiscip. Sci. Rev. 18: 73–80.Google Scholar
  8. Brown MR (1991) The amino acid and sugar composition of 16 species of microalgae used in mariculture. J. exp. mar. Biol. Ecol. 145: 79–99.CrossRefGoogle Scholar
  9. Campos JL, Figueras X, Pinol MT, Boronat A, Tiburcio AF (1991) Carotenoid and conjugated polyamine levels as indicators of ultraviolet-C induced stress in Arabidopsis thaliana. Photochem. Photobiol. 53: 689–693.CrossRefGoogle Scholar
  10. Chandler SF, Dodds JH (1983) The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasidine in callus cultures of Solanum laciniatum. Plant Cell Rep. 2: 105.CrossRefGoogle Scholar
  11. Chavan UD, Amarowicz R, Shahidi F (1999) Antioxidant activity and phenolic fractions of beach pea (Lathyrus maritimus L.). J. Food Lipids. 6: 1–11.Google Scholar
  12. Duval B, Duval E, Hoham RW (1999) Snow algae of the Sierra Nevada, Spain, and the High Atlas Mountains of Morocco. Microbiol. Intl. 2: 39–42.Google Scholar
  13. Floss HG (1997) Natural products derived from unusual variants of the shikimate pathway. Natural Prod. Rep. 14: 433–452.CrossRefGoogle Scholar
  14. Foti M, Piattelli M, Amico V, Ruberto G (1994) Antioxidant activity of phenolic meroditerpenoids from marine algae. J. Photochem. Photobiol. 26: 159–164.CrossRefGoogle Scholar
  15. Fritzemeier K-H, Rolfs C-H, Pfau J, Kindi, H (1983) Action of ultraviolet-C on stilbene formation in callus of Arachis hypogaea. Planta. 159: 25–29.CrossRefGoogle Scholar
  16. Gerber S, Häder D-P (1994) Effects of enhanced UV-B irradiation on the red coloured freshwater flagellate Euglena sanguinea. FEMS Microbiol. Ecol. 13: 177–184.CrossRefGoogle Scholar
  17. Gerwick WH, Roberts MA, Proteau JP, Chen J-L (1994) Screening cultured marine microalgae for anticancer-type activity. J. appl. Phycol. 6: 143–149.CrossRefGoogle Scholar
  18. Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul. 21: 79–102.CrossRefGoogle Scholar
  19. Hoham RW, Duval B (2000) Microbial ecology of snow and fresh-water ice with emphasis on snow algae. In Jones HG, Pomeroy JW, Walker DA, Hoham RW (eds), Snow Ecology: An Interdisciplinary Examination of Snow-Covered Ecosystems. Cambridge Univ. Press, Cambridge, UK (in press).Google Scholar
  20. Hoppe H, (1982) Marine algae: their products and constituents. In Hoppe H, Lovring T (eds), Marine Algae in Pharmaceutical Science. Vol 2. Walter de Gruyter, Berlin, pp. 3–48.Google Scholar
  21. Huang M-T, Farraro T (1992) Phenolic compounds in food and cancer prevention. In Huang M-T, Ho C-T, Lee CY (eds), Phenolic compounds in food and their effects on health II, antioxidants and cancer prevention. Chap 2. ACS Sym 507: 8–33.Google Scholar
  22. Jorgensen LV, Madsen HL, Thomsen MK, Dragsted LO, Skibsted LH (1999) Regulation of phenolic antioxidants from phenoxyl radicals: An ESR and electrochemical study of antioxidant hierarchy. Free Radical Res. 30: 207–220.Google Scholar
  23. Kol E (1968) Kryobiologie. Biologie und Limnologie des Schnees und Eises. I. Kryovegetation. In Elster HJ, Ohle W (eds), Die Binnengewasser, E. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart: 216 pp.Google Scholar
  24. König GM, Wright AD (1993) Algal secondary metabolites and their pharmaceutical potential. In Kinghorn AD, Balandrin MF (eds), Human medicinal agents from plants. ACS Washington D.C., pp. 276–293.Google Scholar
  25. Kozak RG, Ricco RA, Gurni AA, Boveris AD, Puntarulo S (1999) Antioxidant response of soybean cotyledons (Glycine max) to ultraviolet irradiation. Can. J. Plant Sci. 79: 181–189.Google Scholar
  26. Kwok D, Shetty K (1997) Effects of proline and proline analogs on total phenolic and rosmarinic acid levels in shoot clones of thyme (Thymus vulgaris L). J. Food Biochem. 22: 37–51.Google Scholar
  27. Liu L, Gitz DC, McClure JW (1995) Effects of UV-B on flavonoids, ferulic acid, growth and photosynthesis in barley primary leaves. Physiol. Plant. 93: 725–733.CrossRefGoogle Scholar
  28. Lohrenz SE, Taylor CD (1987) Inorganic 14C as a probe of growth rate-dependent variations in intracellular free amino acid and protein composition of NH4-limited continuous cultures of Nannochloris atomis B. J. Exp. Mar. Biol. Ecol. 106: 31–55.CrossRefGoogle Scholar
  29. Malanga G, Puntarulo S (1995) Oxidative stress and antioxidant content in Chlorella vulgaris after exposure to ultraiolet-B radiation. Physiol. Planta. 94: 672–679.CrossRefGoogle Scholar
  30. Marchant HJ (1998) Life in the snow: algae and other microorganisms. In Green K (ed.), Snow: A Natural History; an Uncertain Future. Australian Alps Liaison Committee, Canberra, Australia. Chap. 5, pp. 83–97.Google Scholar
  31. Margalith PZ (1992) Pigment Microbiology. Chapman and Hall, London, 156 pp.Google Scholar
  32. Müller T, Bleiß W, Rogaschewski MS, Fuhr G (1998) Snow algae from northwest Svalbard: their identification, distribution, pigment and nutrient content. Polar Biol. 20: 14–32.CrossRefGoogle Scholar
  33. Paganga G, Miller N, Rice-Evans CA (1999) The polyphenolic content of fruit and vegetables and their antioxidant activities. What does a serving constitute? Free Radical Res. 30: 153–162.Google Scholar
  34. Pardha SP, Alia AS, Prasad KV (1995) Proline accumulates in plants exposed to UV radiation and protects them against UV induced peroxidation. Biochem. Biophys. Res. Commun. 209: 1–5.CrossRefGoogle Scholar
  35. Piacentini MP, Ricci D, Fraternale D, Piatti E, Manunta A, Accorsi A (1999) Effects of UV-C irradiation on phosphoinositide turnover in plant cells: similarities with those occurring via the formation of reactive oxygen intermediates in animal cells. Comp. Biochem. Physiol. B 122: 293–299.PubMedCrossRefGoogle Scholar
  36. Pratt DE (1992) Natural antioxidants in plant material. In Haung M-T, Ho C-T, Lee CY (eds), Phenolic Compounds in Food and Their Effects on Health II. Antioxidants and Cancer Prevention. Chap. 5. ACS Sym. 507: 55–72.Google Scholar
  37. Reuber S, Bornman JF, Weissenbock G (1996) A flavonoid mutant of barley (Hordeum vulgare L.) exhibits increased sensitivity of UV-B radiation in the primary leaf. Plant Cell Environ. 19: 593–601.CrossRefGoogle Scholar
  38. Rice-Evans CA, Miller NJ, Bolwell PG, BramLey PM, Pridham JB (1995) The relative antioxidant activities of plant-derived polyphenolic flavonoids. Free Rad. Res. 22: 375–383.CrossRefGoogle Scholar
  39. Setchell KD, Lawson AM, Borriello SP, Harkness R, Gordon H, Morgan DM (1981) Lignan formation in man-microbial involvement and possible roles in relation to cancer. Lancet. 2: 4–7.PubMedCrossRefGoogle Scholar
  40. Shetty K (1997) Biotechnology to harness the benefits of dietary phenolics; focus on Lamiaceae. Asia Pacific J. Clin. Nutr. 6: 162–171.Google Scholar
  41. Shetty K, Curtis OF, Levin RE, Witkowsky R, Ang V (1995) Prevention of vitrification associated with the in vitro shoot culture of oregano (Origanum vulgare) by Psuedomonas spp. J. Plant Physiol. 147: 447–451.Google Scholar
  42. Sommaruga R, Garcia-Pichel F (1999) UV-absorbing mycosproinelike compounds in planktonic and benthic organisms from a high-mountain lake. Arch. Hydrobiol. 144: 255–269.Google Scholar
  43. Tevini M (1993) Effects of enhanced UV-B radiation on terrestrial plants. In Tevini M (ed.), UV-B Radiation and Ozone Depletion. Lewis Publ., Boca Raton, FL: pp. 125–153.Google Scholar
  44. Thomas WH (1972) Observations on snow algae in California. J. Phycol. 8: 1–9.CrossRefGoogle Scholar
  45. Thomas WH, Duval B (1995) Sierra Nevada, California, U.S.A., snow algae: snow albedo changes, algal-bacterial interrelationships, and ultraviolet radiation effects. Arc. Alp. Res. 27: 389–399.CrossRefGoogle Scholar
  46. Thomas WH, Duval B (1996) Effects of microalgal blooms on Sierra Nevada snow albedo. In Proc. 64th Western Snow Conf., Bend, Oregon: pp. 149–154.Google Scholar
  47. Thomas WH, Seibert DLR, Alden M, Eldridge P, Neori A (1984) Yields, photosynthetic efficiencies and proximate composition of dense marine microalgal cultures. I. Introduction and Phaeodactylum tricornutum experiments. Biomass 5: 181–209.CrossRefGoogle Scholar
  48. Wellmann E (1975) UV dose-dependent induction of enzymes related to flavonoid biosynthesis in cell suspension cultures of parsley. FEBS Lett. 51: 105–107.PubMedCrossRefGoogle Scholar
  49. Wynn-Williams DD (1994) Potential effects of ultraviolet radiation on Antarctic primary terrestrial colonizers: cyanobacteria, algae, and cryptogams. Antarc. Res. Ser. 62: 243–257.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Brian Duval
    • 1
  • Kalidas Shetty
    • 2
  • William H. Thomas
    • 3
  1. 1.Environmental Health Sciences, Morrill I N-344University of MassachusettsAmherstUSA
  2. 2.Department of Food ScienceUniversity of MassachusettsAmherstUSA
  3. 3.Scripps Institute of OceanographyUniversity of CaliforniaSan Diego, La JollaUSA

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