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Motility and photosynthetic responses of the green microalga Tetraselmis subcordiformis to visible and UV light levels

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Abstract

To test the effects of photosynthetic active radiation (PAR, 400–700 nm) and ultraviolet radiation (UVR, 280–400 nm) on phototaxis and photosynthesis of free swimming microalgae, experiments were performed with Tetraselmis subcordiformis (Wille) Butcher under a solar simulator. In particular, we evaluated the effects of different PAR levels and radiation regimes (i.e., PAR only and PAR+UVR) on those two processes. We found that the cells preferred to move to a particular area (e.g., receiving 100 W m−2 PAR) with little photochemical suppression or inhibition of carbon fixation. Adding UV-A to high PAR decreased its swimming capacity and photosynthetic capability, and further adding UV-B led to more inhibition. The suppression of the moving capability of T. subcordiformis was reversible but the cells exposed to PAR combined with UVR needed longer time intervals to recover their motility as compared with those irradiated only with PAR. Based on the above results, we postulate that in nature, the motile capability and photosynthesis of free swimming the green microalga might be impaired by enhanced solar UVR. On the other hand, the cells can reduce the damage caused by high irradiances (and even get the optimum light level for photosynthesis) by a behavioral swimming response.

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References

  • Alonso C, Rocco V, Barriga JP, Battini MÁ, Zagarese H (2004) Surface avoidance by freshwater zooplankton: field evidence on the role of ultraviolet radiation. Limnol Oceanogr 49:225–232

    Article  CAS  Google Scholar 

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  PubMed  CAS  Google Scholar 

  • Beardall J, Stojkovic S (2006) Microalgae under global environmental change: implications of growth and productivity, populations and trophic flow. ScienceAsia 32(Suppl):1–10

    Article  Google Scholar 

  • Bebout BM, Garcia-Pichel F (1995) UV-B induced vertical migrations of cyanobacteria in a microbial mat. Appl Environ Microbiol 61:4215–4222

    PubMed  CAS  Google Scholar 

  • Behrenfeld MJ, Lean DRS, Lee H (1995) Ultraviolet-B radiation effects on inorganic nitrogen uptake by natural assemblages of oceanic phytoplankton. J Phycol 31:25–36

    Article  CAS  Google Scholar 

  • Berthold P, Tsunoda SP, Ernst OP, Mages W, Gradmann D, Hegemann P (2008) Channelrhodopsin-1 initiates phototaxis and photophobic responses in Chlamydomonas by immediate light-induced depolarization. Plant Cell 20:1665–1677

    Article  PubMed  CAS  Google Scholar 

  • Bouchard JN, Campbell DA, Roy S (2005) 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 

  • Clegg MR, Maberly SC, Jones RI (2004) Dominance and compromise in freshwater phytoplanktonic flagellates: the interaction of behavioral preferences for conflicting environmental gradients. Funct Ecol 18:371–380

    Article  Google Scholar 

  • Dillon JG, Tatsumi CM, Tandingan PG, Castenholz RW (2002) Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium (Chroococcidiopsis sp.). Arch Microbiol 177:322–331

    Article  PubMed  CAS  Google Scholar 

  • Ebrey TG (2002) A new type of photoreceptor in algae. Proc Natl Acad Sci USA 99:8463–8464

    Article  PubMed  CAS  Google Scholar 

  • Ekelund NGA (1994) Influence of UV-B radiation on photosynthetic light-response curves, absorption spectra and motility of four phytoplankton species. Physiol Plant 91:696–702

    Article  CAS  Google Scholar 

  • Foster KW, Saranak J, Patel N, Zarilli G, Okabe M, Kline T, Nakanishi K (1984) A rhodopsin is the functional photoreceptor for phototaxis in the unicellular eukaryote Chlamydomonas. Nature 311:756–759

    Article  PubMed  CAS  Google Scholar 

  • Franklin LA, Osmond CB, Larkum AWD (2003) Photoinhibition. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer, Dordrecht, pp 351–384

    Chapter  Google Scholar 

  • Gao K, Wu Y, Li G, Wu H, Villafañe VE, Helbling EW (2007) Solar UV radiation drives CO2 fixation in marine phytoplankton: a double-edged sword. Plant Physiol 144:54–59

    Article  PubMed  CAS  Google Scholar 

  • Gao K, Li P, Watanabe T, Helbling EW (2008) Combined effects of ultraviolet radiation and temperature on morphology, photosynthesis and DNA of Arthrospira (Spirulina) platensis. J Phycol 44:777–786

    Article  Google Scholar 

  • Genty B, Briantains JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies on marine planktonic diatoms. I. Cyclotella nana (Hustedt) and Detonula confervaceae (Cleve) Gran. Can J Microbiol 8:229–239

    Article  PubMed  CAS  Google Scholar 

  • Häder D-P, Brodhun B (1991) Effects of ultraviolet radiation on the photoreceptor proteins and pigments in the paraflagellar body of the flagellate, Euglena gracilis. J Plant Physiol 137:641–646

    Article  Google Scholar 

  • Häder D-P, Häder MA (1989) Effects of solar UV-B irradiation on photomovement and motility in photosynthetic and colorless flagellates. Environ Exp Bot 29:273–282

    Article  Google Scholar 

  • Häder D-P, Jori G (2001) Photomovement. Elsevier, Amsterdam, pp 169–183

    Google Scholar 

  • Häder D-P, Worrest RC (1991) Effects of enhanced solar ultraviolet radiation on aquatic ecosystems. Photochem Photobiol 53:717–725

    Article  Google Scholar 

  • Häder D-P, Kumar HD, Smith RC, Worrest RC (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 6:267–285

    Article  PubMed  Google Scholar 

  • Halldal P (1961) Ultraviolet action spectra of positive and negative phototaxis in Platymonas subcordiformis. Physiol Plant 14:133–139

    Article  CAS  Google Scholar 

  • Heraud P, Beardall J (2000) Changes in chlorophyll fluorescence during exposure of Dunaliella tertiolecta to UV radiation indicate a dynamic interaction between damage and repair processes. Photosynth Res 63:123–134

    Article  PubMed  CAS  Google Scholar 

  • Holm-Hansen O, Helbling EW (1995) Técnicas para la medición de la productividad primaria en el fitoplancton. In: Alveal K, Ferrario ME, Oliveira EC, Sar E (eds) Manual de métodos ficológicos. Univ. de Concepción, Chile, pp 329–350

    Google Scholar 

  • Jékely G (2009) Evolution of phototaxis. Phil Trans R Soc B 364:2795–2808

    Article  PubMed  Google Scholar 

  • Karentz D, Cleaver JE, Mitchell DL (1991) Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation. J Phycol 27:326–341

    Article  CAS  Google Scholar 

  • Kramer GF, Norman HA, Krizek DT, Mirecki RM (1991) Influence of UV-B radiation on polyamines, lipid peroxidation and membrane lipids in cucumber. Phytochemistry 30:2101–2108

    Article  CAS  Google Scholar 

  • Kröger O, Hegemann P (1994) Photophobic responses and phototaxis in Chlamydomonas are triggered by a single rhodopsin photoreceptor. FEBS Lett 341:5–9

    Article  PubMed  Google Scholar 

  • Li J, Sun S, Li C, Zhang Z, Pu X (2008) Effects of different diets on the reproduction and nauplia development of the copepod Acartia bifilosa. J Exp Mar Biol Ecol 355:95–102

    Article  Google Scholar 

  • Liu Z, Häder D-P, Sommaruga R (2004) Occurrence of mycosporine like amino acids (MAAs) in the bloom-forming cyanobacterium. Microcystis aeruginosa. J Plankton Res 26:963–966

    Article  CAS  Google Scholar 

  • Ma Z, Gao K (2009) Photosynthetically active and UV radiation act in an antagonistic way in regulating buoyancy of Arthrospira (Spirulina) platensis (cyanobacterium). Environ Exp Bot 66:265–269

    Article  CAS  Google Scholar 

  • Ma Z, Gao K (2010) Spiral breakage and photoinhibition of Arthrospira platensis (Cyanophyta) caused by accumulation of reactive oxygen species under solar radiation. Environ Exp Bot 68:208–213

    Article  CAS  Google Scholar 

  • Ma Z, Li W, Gao K (2010) Horizontal migration of Acartia pacifica Steuer (Copepoda) in response to UV-radiation. J Photochem Photobiol B: Biol 101:233–237

    Article  CAS  Google Scholar 

  • Menck CFM (2002) Shining a light on photolyases. Nat Genet 32:338–339

    Article  PubMed  CAS  Google Scholar 

  • Murphy TM (1983) Membranes as targets of ultraviolet radiation. Physiol Plant 58:381–388

    Article  CAS  Google Scholar 

  • Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM, Bamberg E, Hegemann P (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395–2398

    Article  PubMed  CAS  Google Scholar 

  • Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E (2003) Channelrhodopsin-2, a directly light-gated cation selective membrane channel. Proc Natl Acad Sci USA 100:13940–13945

    Article  PubMed  CAS  Google Scholar 

  • Neale PJ, Kieber DJ (2000) Assessing biological and chemical effects of UV in the marine environment: spectral weighting functions. In: Hester RE, Harrison RM (eds) Causes and environmental implications of increased UV-B radiation. The Royal Society of Chemistry, Cambridge, pp 61–83

    Chapter  Google Scholar 

  • Rhode SC, Pawlowski M, Tollrian R (2001) The impact of ultraviolet radiation on the vertical distribution of zooplankton of the genus Daphnia. Nature 412:69–72

    Article  PubMed  CAS  Google Scholar 

  • Richter PR, Häder D-P, Gonçalves RJ, Marcoval MA, Villafañe VE, Helbling EW (2007) Vertical migration and motility response in three marine phytoplankton species exposed to solar radiation. Photochem Photobiol 83:810–817

    Article  PubMed  CAS  Google Scholar 

  • Sgarbossa A, Checcucci G, Lenci F (2002) Photoreception and photomovements of microorganisms. Photochem Photobiol Sci 1:459–467

    Article  PubMed  CAS  Google Scholar 

  • Sineshchekov OA, Jung KH, Spudich JL (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 99:8689–8694

    PubMed  CAS  Google Scholar 

  • Sinha RP, Häder D-P (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1:225–236

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Takahashi T, Kubota M, Watanabe M, Yoshihara K, Deguini F, Nakanishi K (1992) Diversion of the sign of phototaxis in a Chlamydomonas reinhardtii mutant incorporated with retinal and its analogs. FEBS Lett 314:275–279

    Article  PubMed  CAS  Google Scholar 

  • Tirlapur U, Scheuerlein R, Häder D-P (1993) Motility and orientation of a dinoflagellate, Gymnodinium, impaired by solar and ultraviolet radiation. FEMS Microbiol Lett 102:167–174

    Article  Google Scholar 

  • Villafañe VE, Sundbäck K, Figueroa FL, Helbling EW (2003) Photosynthesis in the aquatic environment as affected by UVR. In: Helbling EW, Zagarese HE (eds) UV effects in aquatic organisms and ecosystems. The Royal Society of Chemistry, Cambridge, pp 357–397

    Chapter  Google Scholar 

  • Villafañe VE, Gao K, Li P, Li G, Helbling EW (2007) Vertical mixing within the epilimnion modulates UVR-induced photoinhibition in tropical phytoplankton from Southern China. Freshw Biol 52:1260–1270

    Article  Google Scholar 

  • Wei E, Berry JA (1987) Quantum efficiency of photosystem II in relation to ‘energy’-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta 894:198–208

    Article  Google Scholar 

  • Wemmer K, Marshall W (2004) Flagellar motility: all pull together. Curr Biol 14:992–993

    Article  Google Scholar 

  • Williamson CE, Olson OG, Lott SE, Walker ND, Engstrom DR, Hargreaves BR (2001) Ultraviolet radiation and zooplankton community structure following deglaciation in Glacier Bay, Alaska. Ecology 82:1748–1760

    Article  Google Scholar 

  • Xie J, Zhang Y, Li Y, Wang Y (2001) Mixotrophic cultivation of Platymonas subcordiformis. J Appl Phycol 13:343–347

    Article  Google Scholar 

  • Yu J, Tang X, Zhang P, Tian J, Cai H (2004) Effects of CO2 enrichment on photosynthesis, lipid peroxidation and activities of antioxidative enzymes of Platymonas subcordiformis subjected to UV-B radiation stress. Acta Bot Sin 46:682–690

    CAS  Google Scholar 

  • Zhang P, Yu J, Tang X (2005) UV-B radiation suppresses the growth and antioxidant systems of two marine microalgae, Platymonas subcordiformis (Wille) Hazen and Nitzschia closterium (Ehrenb.) W. Sm. J Integr Plant Biol 47:683–691

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the comments and suggestions of an anonymous reviewer that helped to improve this manuscript. This study was supported by National Natural Science Foundation (No. 40930846, No. 41120164007), Program for Changjiang Scholars and Innovative Research Team (IRT0941), China–Japan collaboration project from MOST (S2012GR0290). Shanghai Municipal Natural Science Foundation (No. 11ZR1449900) and the visiting professor program for State Key Laboratory of Marine Environmental Science, Xiamen University (MELRS0919); E. Walter Helbling and Virginia E. Villafañe were supported by the visiting professor program (111) from the Ministry of Education. This is contribution no. xx of Estación de Fotobiología Playa Unión.

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Correspondence to Kunshan Gao.

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Ma, Z., Helbling, E.W., Li, W. et al. Motility and photosynthetic responses of the green microalga Tetraselmis subcordiformis to visible and UV light levels. J Appl Phycol 24, 1613–1621 (2012). https://doi.org/10.1007/s10811-012-9822-4

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