Abstract
The effects of acute solar radiation stress on photosynthetic efficiency in freshwater unialgal cultures representing three phytoplankton pigment groups were measured by pulse amplitude modulated fluorometry (Walz Phyto-PAM) and compared to previous observations on field populations. Ultraviolet radiation (UVR) (UV-B and UV-A) induced a loss of photochemical quantum efficiency (Fv/Fm) in all 13 taxa examined in culture, while effects of photosynthetically active radiation (PAR) were smaller and often insignificant. Cyanobacteria were the most sensitive to PAR and UVR stress, chlorophytes the least and chromophytes intermediate but variable. The kinetics of maximal (Fm) and minimal (F0) fluorescence responses suggested uncoupling of antenna pigments from reaction centers (decreased Fm) persistent after dark adaptation was a common response, in particular for chromophytes, while the extent of impairment from damaged reaction centers (increased F0) was more variable. Changes in Fv/Fm with irradiance exposure were well described by the Kok model of photoinhibition and indicated that damage, rather than recovery, processes were predictive of acute cumulative inhibition. Field populations of cyanobacteria and chromophytes tended to greater tolerance and lower damage rates than laboratory strains. The results for cultures under standardized conditions supported field results in showing cyanobacteria more sensitive to acute UVR exposure than eukaryotic algae, and thus lacking any innate resistance of photosystem II to sunlight stress that might help explain their success in surface bloom formation.
Similar content being viewed by others
Abbreviations
- F 0 :
-
Minimal fluorescence
- F v :
-
Variable fluorescence
- F m :
-
Maximal fluorescence
- F v/F m :
-
Maximum quantum yield of photochemistry
- Chl a, b, c :
-
Chlorophyll a, b and c, respectively
- NPQ:
-
Non-photochemical quenching
- P:
-
PAR-only experimental light treatment
- PA:
-
PAR + UV-A experimental light treatment
- PAB:
-
PAR + UV-A + UV-B experimental light treatment
- PAR:
-
Photosynthetically active radiation
- PAM:
-
Pulse amplitude modulation
- PC:
-
Phycocyanin
- PE:
-
Phycoerythrin
- PSII:
-
Photosystem II
- ROS:
-
Reactive oxygen species
- UVR:
-
Ultraviolet radiation
References
Acuña AM, Snellenburg JJ, Gwizdala M, Kirilovsky D, van Grondelle R, van Stokkum IHM (2016) Resolving the contribution of the uncoupled phycobilisomes to cyanobacterial pulse-amplitude modulated (PAM) fluorometry signals. Photosynth Res 127(1):91–102
Andreasson KIM, Wängberg S (2006) Biological weighting functions as a tool for evaluating two ways to measure UVB radiation inhibition on photosynthesis. J Photochem Photobiol B 84(2):111–118. https://doi.org/10.1016/j.jphotobiol.2006.02.004
Beecraft L, Watson SB, Smith REH (2017) Multi-wavelength pulse amplitude modulated fluorometry (Phyto-PAM) reveals differential effects of ultraviolet radiation on the photosynthetic physiology of phytoplankton pigment groups. Freshw Biol 62(1):72–86. https://doi.org/10.1111/fwb.12850
Bouchard J, Roy S, Campbell DA (2006) UVB effects on the photosystem II-D1 protein of phytoplankton and natural phytoplankton communities. Photochem Photobiol 82(4):936–951. https://doi.org/10.1562/2005-08-31-IR-666
Brunet C, Johnsen G, Lavaud J, Roy S (2011) Pigments and photoacclimation processes. In: Roy S, Llewellyn CA, Egeland ES, Johnsen G (eds) Phytoplankton pigments: characterization, chemotaxonomy and applications in oceanography. Cambridge University Press, Cambridge, pp 445–471
Callieri C, Bertoni R, Contesini M, Bertoni F (2014) Lake level fluctuations boost toxic cyanobacterial “oligotrophic blooms”. PLoS ONE 9(10):e109526. https://doi.org/10.1371/journal.pone.0109526
Campbell D, Hurry V, Clarke AK, Gustafsson P, Oquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62(3):667–683
Deblois CP, Marchand A, Juneau P (2013) Comparison of photoacclimation in twelve freshwater photoautotrophs (chlorophyte, bacillaryophyte, cryptophyte and cyanophyte) isolated from a natural community. PLoS ONE 8(3):e57139. https://doi.org/10.1371/journal.pone.0057139
Demers S, Roy S, Gagnon R, Vignault C (1991) Rapid light-induced-changes in cell fluorescence and in xanthophyll-cycle pigments of Alexandrium excavatum (Dinophyceae) and Thalassiosira pseudonana (Bacillariophyceae): a photo-protection mechanism. Mar Ecol Prog Ser 76(2):185–193. https://doi.org/10.3354/meps076185
Dimier C, Corato F, Tramontano F, Brunet C (2007) Photoprotection and xanthophyll-cycle activity in three marine diatoms. J Phycol 43(5):937–947. https://doi.org/10.1111/j.1529-8817.2007.00381.x
Doyle SA, Saros JE, Williamson CE (2005) Interactive effects of temperature and nutrient limitation on the response of alpine phytoplankton growth to ultraviolet radiation. Limnol Oceanogr 50(5):1362–1367
Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, Princeton
Fouqueray M, Mouget J, Morant-Manceau A, Tremblin G (2007) Dynamics of short-term acclimation to UV radiation in marine diatoms. J Photochem Photobiol B 89(1):1–8. https://doi.org/10.1016/j.jphotobiol.2007.07.004
Fragoso GM, Neale PJ, Kana TM, Pritchard AL (2014) Kinetics of photosynthetic response to ultraviolet and photosynthetically active radiation in Synechococcus WH8102 (Cyanobacteria). Photochem Photobiol 90(3):522–532. https://doi.org/10.1111/php.12202
Garcia-Pichel F (1994) A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39(7):1704–1717. https://doi.org/10.4319/lo.1994.39.7.1704
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990(1):87–92
Giordanino VMF, Sebastian SM, Villafane VE, Helbling WE (2011) Influence of temperature and UVR on photosynthesis and morphology of four species of cyanobacteria. J Photochem Photobiol B 103(1):68–77. https://doi.org/10.1016/j.jphotobiol.2011.01.013
Guan W, Li P, Jian JB, Wang JY, Lu SH (2011) Effects of solar ultraviolet radiation on photochemical efficiency of Chaetoceros curvisetus (Bacillariophyceae). Acta Physiol Plant 33(3):979–986. https://doi.org/10.1007/s11738-010-0630-7
Guillard RR, Lorenzen C (1972) Yellow-green algae with chlorophyllide C. J Phycol 8(1):10–14. https://doi.org/10.1111/j.0022-3646.1972.00010.x
Häder DP, Helbling WE, Williamson CE, Worrest RC (2011) Effects of UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 10(2):242–260. https://doi.org/10.1039/c0pp90036b
Halac SR, Guendulain-Garcia SD, Villafane VE, Walter Helbling E, Banaszak AT (2013) Responses of tropical plankton communities from the Mexican Caribbean to solar ultraviolet radiation exposure and increased temperature. J Exp Mar Biol Ecol 445:99–107. https://doi.org/10.1016/j.jembe.2013.04.011
Halac SR, Villafane VE, Goncalves RJ, Helbling WE (2014) Photochemical responses of three marine phytoplankton species exposed to ultraviolet radiation and increased temperature: role of photoprotective mechanisms. J Photochem Photobiol B 141:217–227. https://doi.org/10.1016/j.jphotobiol.2014.09.022
Harrison JW, Smith REH (2011a) Deep chlorophyll maxima and UVR acclimation by epilimnetic phytoplankton. Freshw Biol 56(5):980–992. https://doi.org/10.1111/j.1365-2427.2010.02541.x
Harrison JW, Smith REH (2011b) The spectral sensitivity of phytoplankton communities to ultraviolet radiation-induced photoinhibition differs among clear and humic temperate lakes. Limnol Oceanogr 56(6):2115–2126. https://doi.org/10.4319/lo.2011.56.6.2115
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
Heraud P, Roberts S, Shelly K, Beardall J (2005) Interactions between UV-B exposure and phosphorus nutrition. II. Effects on rates of damage and repair. J Phycol 41(6):1212–1218. https://doi.org/10.1111/j.1529-8817.2005.00149.x
Herrmann H, Hader D, Kofferlein M, Seidlitz H, Ghetti F (1996) Effects of UV radiation on photosynthesis of phytoplankton exposed to solar simulator light. J Photochem Photobiol B 34(1):21–28. https://doi.org/10.1016/1011-1344(95)07245-4
Jakob T, Schreiber U, Kirchesch V, Langner U, Wilhelm C (2005) Estimation of chlorophyll content and daily primary production of the major algal groups by means of multiwavelength-excitation PAM chlorophyll fluorometry: performance and methodological limits. Photosynth Res 83(3):343–361. https://doi.org/10.1007/s11120-005-1329-2
Key T, McCarthy A, Campbell D, Six C, Roy S, Finkel Z (2010) Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environ Microbiol 12(1):95–104. https://doi.org/10.1111/j.1462-2920.2009.02046.x
Kirilovsky D (2015) Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions. Photosynth Res 126(1):3–17. https://doi.org/10.1007/s11120-014-0031-7
Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press, Cambridge
Kok B, Businger JA (1956) Kinetics of photosynthesis and photo-inhibition. Nature 177(4499):135–136. https://doi.org/10.1038/177135a0
Kolbowski J, Schreiber U (1995) Computer-controlled phytoplankton analyzer based on a 4-wavelengths PAM chlorophyll fluorometer. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol V. Kluwer, Dordrecht, pp 825–828
Kulk G, van de Poll WH, Visser RJW, Buma AGJ (2011) Distinct differences in photoacclimation potential between prokaryotic and eukaryotic oceanic phytoplankton. J Exp Mar Biol Ecol 398(1–2):63–72. https://doi.org/10.1016/j.jembe.2010.12.011
Laurion I, Roy S (2009) Growth and photoprotection in three dinoflagellates (including two strains of Alexandrium tamarense) and one diatom exposed to four weeks of natural and enhanced ultraviolet-B radiation. J Phycol 45(1):16–33. https://doi.org/10.1111/j.1529-8817.2008.00618.x
Laurion I, Vincent W (1998) Cell size versus taxonomic composition as determinants of UV-sensitivity in natural phytoplankton communities. Limnol Oceanogr 43(8):1774–1779
Lesser MP, Cullen JJ, Neale PJ (1994) Carbon uptake in a marine diatom during acute exposure to ultraviolet-B radiation: relative importance of damage and repair. J Phycol 30(2):183–192. https://doi.org/10.1111/j.0022-3646.1994.00183.x
Litchman E, Neale P (2005) UV effects on photosynthesis, growth and acclimation of an estuarine diatom and cryptomonad. Mar Ecol Prog Ser 300:53–62. https://doi.org/10.3354/meps300053
Litchman E, Neale P, Banaszak A (2002) Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair. Limnol Oceanogr 47(1):86–94
Lohscheider JN, Strittmatter M, Kuepper H, Adamska I (2011) Vertical distribution of epibenthic freshwater cyanobacterial Synechococcus spp. strains depends on their ability for photoprotection. PLoS ONE 6(5):e20134. https://doi.org/10.1371/journal.pone.0020134
MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38(1):17–38. https://doi.org/10.1046/j.1529-8817.2002.00094.x
MacIntyre HL, Lawrenz E, Richardson TL (2010) Taxonomic discrimination of phytoplankton by spectral fluorescence. In: Suggett David J, Prášil Ondrej, Borowitzka Michael A (eds) Chlorophyll a fluorescence in aquatic sciences methods and applications. Springer, Dordrecht, pp 129–169
Marcoval MA, Villafane VE, Helbling EW (2007) Interactive effects of ultraviolet radiation and nutrient addition on growth and photosynthesis performance of four species of marine phytoplankton. J Photochem Photobiol B 89(2–3):78–87. https://doi.org/10.1016/j.jphotobiol.2007.09.004
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence: a practical guide. J Exp Bot 51(345):659–668. https://doi.org/10.1093/jexbot/51.345.659
Montero O, Klisch M, Hader D, Lubian L (2002a) Comparative sensitivity of seven marine microalgae to cumulative exposure to ultraviolet-B radiation with daily increasing doses. Bot Mar 45(4):305–315. https://doi.org/10.1515/BOT.2002.030
Montero O, Sobrino C, Pares G, Lubian L (2002b) Photoinhibition and recovery after selective short-term exposure to solar radiation of five chlorophyll c-containing marine microalgae. Cienc Mar 28(3):223–236
Moore CM, Suggett D, Hickman A, Kim Y, Tweddle J, Sharples J, Geider R, Holligan P (2006) Phytoplankton photoacclimation and photoadaptation in response to environmental gradients in a shelf sea. Limnol Oceanogr 51(2):936–949. https://doi.org/10.4319/lo.2006.51.2.0936
Neale PJ, Pritchard AL, Ihnacik R (2014) UV effects on the primary productivity of picophytoplankton: biological weighting functions and exposure response curves of Synechococcus. Biogeosciences 11(10):2883–2895. https://doi.org/10.5194/bg-11-2883-2014
Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta Bioenerg 1757(7):742–749. https://doi.org/10.1016/j.bbabio.2006.05.013
Paerl HW, Kellar PE (1979) Nitrogen-fixing anabaena: physiological adaptations instrumental in maintaining surface blooms. Science 204(4393):620–622. https://doi.org/10.1126/science.204.4393.620
Paerl HW, Paul VJ (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Res 46(5):1349–1363. https://doi.org/10.1016/j.watres.2011.08.002
Phinney D, Yentsch C (1985) A novel phytoplankton chlorophyll technique: toward automated-analysis. J Plankton Res 7(5):633–642. https://doi.org/10.1093/plankt/7.5.633
Qin H, Li S, Li D (2015) Differential responses of different phenotypes of Microcystis (Cyanophyceae) to UV-B radiation. Phycologia 54(2):118–129. https://doi.org/10.2216/PH14-93.1
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ragni M, Airs RL, Leonardos N, Geider RJ (2008) Photoinhibition of PSII in Emiliania huxleyi (Haptophyta) under high light stress: the roles of photoacclimation, photoprotection, and photorepair. J Phycol 44(3):670–683. https://doi.org/10.1111/j.1529-8817.2008.00524.x
Richardson TL, Lawrenz E, Pinckney JL, Guajardo RC, Walker EA, Paerl HW, MacIntyre HL (2010) Spectral fluorometric characterization of phytoplankton community composition using the Algae Online Analyser (R). Water Res 44(8):2461–2472. https://doi.org/10.1016/j.watres.2010.01.012
Schmitt-Jansen M, Altenburger R (2008) Community-level microalgal toxicity assessment by multiwavelength-excitation PAM fluorometry. Aquat Toxicol 86(1):49–58. https://doi.org/10.1016/j.aquatox.2007.10.001
Schreiber U (1998) Chlorophyll fluorescence: new instruments for special applications. In: Garab G (ed) Photosynthesis: mechanisms and effects. Springer, Dordrecht
Schuurmans RM, van Alphen P, Schuurmans JM, Matthijs HCP, Hellingwerf KJ, Chauvat F (2015) Comparison of the photosynthetic yield of cyanobacteria and green algae: different methods give different answers. PLOS ONE 10(9):e0139061
Schwaderer AS, Yoshiyama K, de Tezanos Pinto P, Swenson NG, Klausmeier CA, Litchman E (2011) Eco-evolutionary differences in light utilization traits and distributions of freshwater phytoplankton. Limnol Oceanogr 56(2):589–598. https://doi.org/10.4319/lo.2011.56.2.0589
Selmeczy GB, Tapolczai K, Casper P, Krienitz L, Padisak J (2016) Spatial- and niche segregation of DCM-forming cyanobacteria in Lake Stechlin (Germany). Hydrobiologia 764(1):229–240. https://doi.org/10.1007/s10750-015-2282-5
Shelly K, Heraud P, Beardall J (2002) Nitrogen limitation in Dunaliella tertiolecta (Chlorophyceae) leads to increased susceptibility to damage by ultraviolet-B radiation but also increased repair capacity. J Phycol 38(4):713–720. https://doi.org/10.1046/j.1529-8817.2002.01147.x
Six C, Sherrard R, Lionard M, Roy S, Campbell DA (2009) Photosystem II and pigment dynamics among ecotypes of the green alga Ostreococcus. Plant Physiol 151(1):379–390. https://doi.org/10.1104/pp.109.140566
Sobrino C, Neale PJ, Lubian LM (2005) Interaction of UV radiation and inorganic carbon supply in the inhibition of photosynthesis: spectral and temporal responses of two marine picoplankton. Photochem Photobiol 81(2):384–393. https://doi.org/10.1562/2004-08-27-RA-295.1
Sommaruga R, Chen Y, Liu Z (2009) Multiple strategies of bloom-forming Microcystis to minimize damage by solar ultraviolet radiation in surface waters. Microb Ecol 57(4):667–674. https://doi.org/10.1007/s00248-008-9425-4
Stamenkovic M, Hanelt D (2011) Growth and photosynthetic characteristics of several Cosmarium strains (Zygnematophyceae, Streptophyta) isolated from various geographic regions under a constant light-temperature regime. Aquat Ecol 45(4):455–472. https://doi.org/10.1007/s10452-011-9367-7
van Donk E, Faafeng B, de Lange H, Hessen D (2001) Differential sensitivity to natural ultraviolet radiation among phytoplankton species in Arctic lakes (Spitsbergen, Norway). Plant Ecol 154(1–2):247–259. https://doi.org/10.1023/A:1012978328768
Wagner H, Jakob T, Wilhelm C (2006) Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytol 169(1):95–108. https://doi.org/10.1111/j.1469-81.7.2005.01550.x
Watson SB (1999) Outbreaks of taste/odour causing algal species: theoretical, mechanistic and applied approaches. Doctor of Philosophy, Biological Sciences, University of Calgary, Calgary, Alberta
Willame R, Boutte C, Grubisic S, Wilmotte A, Komarek J, Hoffmann L (2006) Morphological and molecular characterization of planktonic cyanobacteria from Belgium and Luxembourg. J Phycol 42(6):1312–1332. https://doi.org/10.1111/j.1529-8817.2006.00284.x
Williamson CE, Zepp RG, Lucas RM, Madronich S, Austin AT, Ballare CL, Norval M, Sulzberger B, Bais AF, McKenzie RL, Robinson SA, Häder D, Paul ND, Bornman JF (2014) Solar ultraviolet radiation in a changing climate. Nat Clim Change 4(6):434–441. https://doi.org/10.1038/NCLIMATE2225
Wong C, Teoh M, Phang S, Lim P, Beardall J (2015) Interactive effects of temperature and UV radiation on photosynthesis of Chlorella strains from polar, temperate and tropical environments: differential impacts on damage and repair. PLoS ONE 10(10):e0139469. https://doi.org/10.1371/journal.pone.0139469
Wu X, Kong F, Zhang M (2011) Photoinhibition of colonial and unicellular Microcystis cells in a summer bloom in Lake Taihu. Limnology 12(1):55–61. https://doi.org/10.1007/s10201-010-0321-5
Wulff A, Mohlin M, Sundback K (2007) Intraspecific variation in the response of the cyanobacterium Nodularia spumigena to moderate UV-B radiation. Harmful Algae 6(3):388–399. https://doi.org/10.1016/j.hal.2006.11.003
Xenopoulos MA, Frost PC (2003) UV radiation, phosphorus, and their combined effects on the taxonomic composition of phytoplankton in a boreal lake. J Phycol 39(2):291–302
Xenopoulos MA, Prairie YT, Bird DF (2000) Influence of ultraviolet-B radiation, stratospheric ozone variability, and thermal stratification on the phytoplankton biomass dynamics in a mesohumic lake. Can J Fish Aquat Sci 57(3):600–609. https://doi.org/10.1139/cjfas-57-3-600
Xenopoulos MA, Leavitt PR, Schindler DW (2009) Ecosystem-level regulation of boreal lake phytoplankton by ultraviolet radiation. Can J Fish Aquat Sci 66(11):2002–2010. https://doi.org/10.1139/F09-119
Xiong F, Nedbal L, Neori A (1999) Assessment of UV-B sensitivity of photosynthetic apparatus among microalgae: short-term laboratory screening versus long-term outdoor exposure. J Plant Physiol 155(1):54–62
Yentsch C, Yentsch C (1979) Fluorescence spectral signatures: characterization of phytoplankton populations by the use of excitation and emission-spectra. J Mar Res 37(3):471–483
Zeeshan M, Prasad SM (2009) Differential response of growth, photosynthesis, antioxidant enzymes and lipid peroxidation to UV-B radiation in three cyanobacteria. S Afr J Bot 75(3):466–474. https://doi.org/10.1016/j.sajb.2009.03.003
Zhang M, Kong F, Wu X, Xing P (2008) Different photochemical responses of phytoplankters from the large shallow Taihu Lake of subtropical China in relation to light and mixing. Hydrobiologia 603:267–278. https://doi.org/10.1007/s10750-008-9277-4
Acknowledgements
The main funding for this research was from an NSERC Discovery Grant (R. Smith), with important additional support from Environment and Climate Change Canada (S. Watson).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Télesphore Sime-Ngando.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Beecraft, L., Watson, S.B. & Smith, R.E.H. Innate resistance of PSII efficiency to sunlight stress is not an advantage for cyanobacteria compared to eukaryotic phytoplankton. Aquat Ecol 53, 347–364 (2019). https://doi.org/10.1007/s10452-019-09694-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-019-09694-4