Skip to main content

Differential responses of Nostoc sphaeroides and Arthrospira platensis to solar ultraviolet radiation exposure

Abstract

During October to December 2003 we carried out experiments to assess the impact of high solar radiation levels (as normally occurring in a tropical region of Southern China) on the cyanobacteria Nostoc sphaeroides and Arthrospira (Spirulina) platensis. Two types of experiments were done: a) Short-term (i.e., 20 min) oxygen production of samples exposed to two radiation treatments (i.e., PAR+UVR—280–700 nm, and PAR only—400–700 nm, PAB and P treatments, respectively), and b) Long-term (i.e., 12 days) evaluation of photosynthetic quantum yield (Y) of samples exposed to three radiation treatments (i.e., PAB; PA (PAR+UV-A, 320–700 nm) and P treatments, respectively). N. sphaeroides was resistant to UVR, with no significant differences (P>0.05) in oxygen production within 20 min of exposure, but with a slight inhibition of Y within hours. A fast recovery of Y was observed after one day even in samples exposed to full solar radiation. A. platensis, on the other hand, was very sensitive to solar radiation (mainly to UV-B), as determined by oxygen production and Y measurements. A. platensis had a circadian rhythm of photosynthetic inhibition, and during the first six days of exposure to solar radiation, it varied between 80 and 100% at local noon, but cells recovered significantly during afternoon hours. There was a significant decrease in photosynthetic inhibition after the first week of exposure with values less than 50% at local noon in samples receiving full solar radiation. Samples exposed to PA and P treatments recovered much faster (within 2–3 days), and there were no significant differences in Y between the three radiation treatments when irradiance was low (late afternoon to early morning). Long-term acclimation seems to be important in A. platensis to cope with high UVR levels however, it is not attained through the synthesis of UV-absorbing compounds but it seems to be mostly related to adaptive morphological changes.

This is a preview of subscription content, access via your institution.

Abbreviations

Fm:

Maximal fluorescence in dark-adapted cells (all reaction centers are closed)

Fo:

Initial chlorophyll fluorescence in dark-adapted cells (all reaction centers are open)

Fv:

Variable fluorescence (= Fm-Fo)

Fo':

Fm' and Fv': The same for light-adapted state

Ft:

Current fluorescence of light-adapted cells

PAR:

Photosynthetic Active radiation (400–700 nm)

UV-A:

Ultraviolet-A radiation (315–400 nm)

UV-B:

Ultraviolet-B radiation (280–315 nm)

UVR:

Ultraviolet radiation (280–400 nm)

Y:

Fv'/Fm': Quantum yield (Genty-parameter).

References

  • Banaszak AT (2003) Photoprotective physiological and biochemical responses of aquatic organisms. In: Helbling EW and Zagarese HE (ed.) UV effects in aquatic organisms and ecosystems. The Royal Society of Chemistry, Cambridge, pp. 329–356.

    Chapter  Google Scholar 

  • Caldwell MM, Teramura AH, Tevini M, Bornman JF, Björn LO, Kulandaivelu G (1995) Effects of increased solar ultraviolet radiation on terrestrial plants. Ambio. 24: 166–173.

    Google Scholar 

  • Dunlap WC, Rae GA, Helbling EW, Villafañe VE, Holm-Hansen O (1995) Ultraviolet-absorbing compounds in natural assemblages of Antarctic phytoplankton. Antarct J. US. 30: 323–326.

    Google Scholar 

  • Ehling-Schulz M, Scherer S (1999) UV protection in cyanobacteria. Eur. J Phycol. 34: 329–338.

    Article  Google Scholar 

  • Eker APM, Kooiman P, Hessels JKC, Yasui A (1990) DNA photoreactivating enzyme from the cyanobacterium Anacystis nidulans. J. Biol. Chem. 265: 8009–8015.

    PubMed  CAS  Google Scholar 

  • Figueroa FL, Salles S, Aguilera J, Jiménez C, Mercado J, Viñegla B, Flores-Moya A, Altamirano M (1997) Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta. Mar. Ecol. Prog. Ser. 151: 81–90.

    Article  CAS  Google Scholar 

  • Franklin LA, Forster RM (1997) The changing irradiance environment: Consequences for marine macrophyte physiology, productivity and ecology. Eur. J. Phycol. 32: 207–232.

    Google Scholar 

  • Gao K, Ai H (2004) Relationship of growth and photosynthesis with colony size in an edible cyanobacterium, Ge-Xian–Mi Nostoc (Cyanophyceae). J. Phycol. 40: 523–526.

    Article  Google Scholar 

  • Garcia-Pichel F (1994) A model for internal shelf-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol. Oceanogr. 39: 1704–1717.

    Article  Google Scholar 

  • Garcia-Pichel F (1998) Solar ultraviolet and the evolutionary history of cyanobacteria. Origins of life and evolution of the biosphere, 28: 321–347.

    Article  PubMed  CAS  Google Scholar 

  • Genty BE, Briantais JM, Baker NR (1989) Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-photorespiratory conditions. Plant Physiol. Biochem 28: 1–10.

    Google Scholar 

  • Hanelt D (1996) Photoinhibition of photosynthesis in marine macroalgae. Scientia Marina 60: 243–248.

    CAS  Google Scholar 

  • Holm-Hansen O, Riemann B (1978) Chlorophyll a determination: improvements in methodology. Oikos 30: 438–447.

    Article  CAS  Google Scholar 

  • Korbee Peinado N, Abdala Díaz RT, Figueroa FL, Helbling EW (2004) Ammonium and UV radiation stimulate the accumulation of mycosporine like amino acids in Porphyra columbina (Rhodophyta) from Patagonia, Argentina. J. Phycol. 40: 248–259.

    Article  CAS  Google Scholar 

  • Lu C, Vonshak A (1999) Photoinhibition in outdoor Spirulina platensis cultures assessed by polyphasic chlorophyll fluorescence transients. J. Appl. Phycol. 11: 355–359.

    Article  Google Scholar 

  • Marwood CA, Smith REH, Furgal JA, Charlton MN, Solomon KR, Greenberg BM (2000) Photoinhibition of natural phytoplankton assemblages in Lake Erie exposed to solar ultraviolet radiation. Can. J. Fish. Aquat. Sci. 57: 371–379.

    Article  CAS  Google Scholar 

  • Miyake C, Michihata F, Asada K (1991) Scavenging of hydrogen peroxide in prokaryotic and eukaryotic algae: Acquisition of ascorbate peroxidase during the evolution of cyanobacteria. Plant Cell Physiol. 32: 33–43.

    CAS  Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR, Bowyer JR (ed.) Photoinhibition of photosynthesis, from molecular mechanisms to the field. Bios Scientific Publ., Oxford, pp. 1–24.

    Google Scholar 

  • Qiu B, Liu J, Liu Z, Liu S (2002) Distribution and ecology of the edible cyanobacterium Ge-Xian Mi (Nostoc) in rice fields of Hefeng County in China. J. Appl. Phycol. 423–429.

  • Quesada A, Vincent WF (1997) Strategies of adaptation by Antarctic cyanobacteria to ultraviolet radiation. Eur. J. Phycol. 32: 335–342.

    Article  Google Scholar 

  • Rajagopal S, Jha IB, Murthy SDS, Mohanthy P (1998) Ultraviolet-B effects on Spirulina platensis cells: Modification of chromophore-protein interaction and energy transfer characteristics of phycobilisomes. Biochem. Biophys. Res. Commun. 249: 172–177.

    Article  PubMed  CAS  Google Scholar 

  • Rajagopal S, Murthy SDS, Mohanthy P (2000) Effect of ultraviolet-B radiation on intact cells of the cyanobacterium Spirulina platensis: Characterization of the alterations in the thylakoid membranes. J. Photochem. Photobiol. B. Biol. 54: 61–66.

    Article  CAS  Google Scholar 

  • Sass L, Spetea C, Máté Z, Nagy F, Vass I (1997) Repair of UV-B induced damage of photosystem II via de novo synthesis of the D1 and D2 reaction centre subunits of Scynechocystis sp. PCC 6803. Photosyn. Res. 55–62.

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosyn. Res. 10: 51–62.

    Article  CAS  Google Scholar 

  • Sinha RP, Häder DP (1996) Photobiology and ecophysiology of rice field cyanobacteria. Photochem. Photobiol. 64: 887–896.

    Article  CAS  Google Scholar 

  • Sinha RP, Helbling EW, Häder DP (2003) Effects of solar radiation on photosynthetic quantum yield of a cyanobacterium Nostoc sp. Trends Photochem. Photobiol. 10: 159–166.

    CAS  Google Scholar 

  • Sinha RP, Klisch M, Groniger A, Häder DP (2001a) Responses of aquatic algae and cyanobacteria to solar UV-B. Plant Ecol. 154: 221–236.

    Article  Google Scholar 

  • Sinha RP, Klisch M, Helbling EW, Häder DP (2001b) Induction of mycosporine-like amino acids (MAAs) in cyanobacteria by solar ultraviolet-B radiation. J. Photochem. Photobiol.: B. Biol. 60: 129–135.

    Article  CAS  Google Scholar 

  • Sobrino C, Montero O, Lubián LM (2004) UV-B radiation increases cell permeability and damages nitrogen incorporation mechanisms in Nannochloropsis gaditana. Aquat. Sci. 66: 421–429.

    Article  Google Scholar 

  • Stanier RY, Kunisawa MM, and Cohen-Bazre G (1971) Purification and properties of unicellular blue-green algae (order Chlorococcales). Bact. Rev. 35: 171–201.

    PubMed  CAS  Google Scholar 

  • Villafañe VE, Barbieri ES, Helbling EW (2004) Annual patterns of ultraviolet radiation effects on temperate marine phytoplankton off Patagonia, Argentina. J. Plank. Res. 26: 167–174.

    Article  CAS  Google Scholar 

  • Villafañe VE, Gao K, Helbling EW (2005) Short- and long-term effects of solar ultraviolet radiation on the red algae Porphyridium cruentum (S. F. Gray) Nägeli. Photochem. Photobiol. Sci. 4: 376–382.

    Article  PubMed  CAS  Google Scholar 

  • Villafañe VE, Reid FMH (1995) Métodos de microscopía para la cuantificación del fitoplancton. In: Alveal K Ferrario ME Oliveira EC, Sar E (ed.) Manual de Métodos Ficológicos. Universidad de Concepción, Concepción, Chile, pp. 169–185.

    Google Scholar 

  • Vonshak A (1990) Recent advances in microalgal biotechnology. Biotechnol. Adv. 8: 709–727.

    Article  PubMed  CAS  Google Scholar 

  • Vonshak A, Tomaselli L (2000) Arthrospira (Spirulina): Systematics and ecophysiology. In: Whitton BA, Potts M (ed.) The ecology of cyanobacteria. Academic Publishers, Dordrecht, pp. 505–522.

    Google Scholar 

  • Weis E, Berry A (1987) Quantum efficiency of photosystem II in relation to the energy dependent quenching of chlorophyll fluorescence. Biochim. Biophys. Acta. 894: 198–208.

    Article  CAS  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 144: 307–313.

    CAS  Google Scholar 

  • Wu H, Gao K, Villafañe VE, Watanabe T, Helbling EW (2005) Effects of solar UV radiation and photosynthesis of the filamentous cyanobacterium, Arthrospira platensis. Appl. Environ. Microbiol. 71: 5004–5013.

    Article  PubMed  CAS  Google Scholar 

  • Zar JH (1984) Biostatistical analysis. Prentice Hall, Englewood Cliffs, NJ.

    Google Scholar 

  • Zarrouk C (1966) Contribution a l'étude du cyanophycée. Influence de divers facteurs physiques et chimiques sur la croissance et la photosynthése de Spirulina maxima (Setch et Gardner) Geitl. Ph.D Thesis University of Paris, Paris, France.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Walter Helbling.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Helbling, E.W., Gao, K., Ai, H. et al. Differential responses of Nostoc sphaeroides and Arthrospira platensis to solar ultraviolet radiation exposure. J Appl Phycol 18, 57–66 (2006). https://doi.org/10.1007/s10811-005-9015-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-005-9015-5

Key words

  • Arthrospira platensis
  • cyanobacteria
  • Nostoc sphaeroides
  • oxygen evolution
  • photosynthesis
  • Spirulina
  • UVR