Journal of Oceanology and Limnology

, Volume 36, Issue 6, pp 2194–2201 | Cite as

Effects of the heavy metal cadmium on photosynthetic activity and the xanthophyll cycle in Phaeodactylum tricornutum

  • Yan Ji (季琰)
  • Xiujun Xie (解修俊)
  • Guangce Wang (王广策)Email author


Cadmium (Cd) is one of the most common and widespread heavy metals in the environment. Cd has adverse effects on photosynthesis that are countered by photosystem I (PSI) and photosystem II (PSII); however, the protective responses of these photosystems to heavy metal stress remain unclear. Using the model diatom Phaeodactylum tricornutum, a biological indicator that is widely used to assess the impact of environmental toxins, we simultaneously measured the effects of Cd on PSI and PSII and examined the levels of pigments in response to high light treatments before and after Cd exposure. Cd significantly reduced the quantum yield and electron transport rates of PSI and PSII. The quantum yield of non-photochemical energy dissipation in PSI due to donor side limitation increased faster than the quantum yield due to acceptor side limitation. The Cd treatment activated the P. tricornutum xanthophyll cycle under artificial light conditions, as indicated by an increased diatoxanthin content. Xanthophyll is important for photoprotection; therefore, the accumulation of diatoxanthin may down-regulate PSII activities to reduce oxidative damage. Together, our results suggest that the rapid reduction in PSII activities following Cd exposure is an adaptive response to heavy metal stress that reflects the variable exposure to external stressors in the native P. tricornutum environment.


heavy metal cadmium photosystem I photosystem II Phaeodactylum tricornutum 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



We thank Shelley Robison, PhD, from Liwen Bianji, Edanz Group China (, for editing the English text of a draft of this manuscript.


  1. Bertrand M, Schoefs B, Siffel P, Rohacek K, Molnar I. 2001. Cadmium inhibits epoxidation of diatoxanthin to diadinoxanthin in the xanthophyll cycle of the marine diatom Phaeodactylum tricornutum. FEBS Letters, 508 (1): 153–156.Google Scholar
  2. Biller D V, Bruland K W. 2012. Analysis of Mn, Fe, Co, Ni, Cu, Zn, Cd, and Pb in seawater using the Nobias–chelate PA1 resin and magnetic sector inductively coupled plasma mass spectrometry (ICP–MS). Marine Chemistry, 130–131: 12–20.Google Scholar
  3. Clemens S, Ma J F. 2016. Toxic heavy metal and metalloid accumulation in crop plants and foods. Annual Review of Plant Biology, 67: 489–512.Google Scholar
  4. Deng C N, Zhang D Y, Pan X L, Chang F Q, Wang S Z. 2013. Toxic effects of mercury on PSI and PSII activities, membrane potential and transthylakoid proton gradient in Microsorium pteropus. Journal of Photochemistry and Photobiology B: Biology, 127: 1–7.Google Scholar
  5. Dewez D, Geoffroy L, Vernet G, Popovic R. 2005. Determination of photosynthetic and enzymatic biomarkers sensitivity used to evaluate toxic effects of copper and fludioxonil in alga Scenedesmus obliquus. Aquatic Toxicology, 74 (2): 150–159.Google Scholar
  6. Fargašová A, Bumbálová A, Havránek E. 1999. Ecotoxicological effects and uptake of metals (Cu +, Cu 2+, Mn 2+, Mo 6+, Ni 2+, V 5+ ) in freshwater alga Scenedesmus quadricauda. Chemosphere, 38 (5): 1 165–1 173.Google Scholar
  7. Gao S, Shen S D, Wang G C, Niu J F, Lin A P, Pan G H. 2011. PSI–driven cyclic electron flow allows intertidal macroalgae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant and Cell Physiology, 52 (5): 885–893.Google Scholar
  8. Goss R, Lepetit B. 2015. Biodiversity of NPQ. Journal of Plant Physiology, 172: 13–32.Google Scholar
  9. Guanzon N G, Nakahara H, Yoshida Y. 1994. Inhibitory effects of heavy metals on growth and photosynthesis of three freshwater microalgae. Fisheries Science, 60 (4): 379–384.Google Scholar
  10. Huang W, Yang S J, Zhang S B, Zhang J L, Cao K F. 2011. Cyclic electron flow plays an important role in photoprotection for the resurrection plant Paraboea rufescens under drought stress. Planta, 235 (4): 819–828.Google Scholar
  11. Huang W, Zhang S B, Cao K F. 2010. Stimulation of cyclic electron flow during recovery after chilling–induced photoinhibition of PSII. Plant and Cell Physiology, 51 (11): 1 922–1 928.Google Scholar
  12. Kapkov V I, Belenikina O A, Fedorov V D. 2011. Effect of heavy metals on marine phytoplankton. Moscow University Biological Sciences Bulletin, 66 (1): 32–36.Google Scholar
  13. Klughammer C, Schreiber U. 1994. An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700 +–absorbance changes at 830 nm. Planta, 192 (2): 261–268.Google Scholar
  14. Klughammer C, Schreiber U. 2008. Saturation pulse method for assessment of energy conversion in PS I. PAM Appl ication Notes, 1: 11–14.Google Scholar
  15. Kola H, Wilkinson K J. 2005. Cadmium uptake by a green alga can be predicted by equilibrium modelling. Environ mental Sci ence & Technology, 39 (9): 3 040–3 047.Google Scholar
  16. Lepetit B, Gélin G, Lepetit M, Sturm S, Vugrinec S, Rogato A, Kroth P G, Falciatore A, Lavaud J. 2017. The diatom Phaeodactylum tricornutum adjusts nonphotochemical fluorescence quenching capacity in response to dynamic light via fine–tuned Lhcx and xanthophyll cycle pigment synthesis. New Phytologist, 214 (1): 205–218.Google Scholar
  17. Masmoudi S, Nguyen–Deroche N, Caruso A, Ayadi H, Morant–Manceau A, Tremblin G, Bertrand M, Schoefs B. 2013. Cadmium, copper, sodium and zinc effects on diatoms: from heaven to hell–a review. Cryptogamie, Algologie, 34 (2): 185–225.Google Scholar
  18. Miao A J, Wang W X. 2006. Cadmium toxicity to two marine phytoplankton under different nutrient conditions. Aquatic Toxicology, 78 (2): 114–126.Google Scholar
  19. Monteiro C M, Fonseca S C, Castro P M L, Malcata F X. 2011. Toxicity of cadmium and zinc on two microalgae, Scenedesmus obliquus and Desmodesmus pleiomorphus, from Northern Portugal. Journal of Applied Phycology, 23 (1): 97–103.Google Scholar
  20. Naser H A. 2013. Assessment and management of heavy metal pollution in the marine environment of the Arabian Gulf: a review. Marine Pollution Bulletin, 72 (1): 6–13.Google Scholar
  21. Nawrot T, Plusquin M, Hogervorst J, Roels P A, Celis H, Thijs L, Vangronsveld J, Van Hecke E, Staessen J A. 2006. Environmental exposure to cadmium and risk of cancer: a prospective population–based study. The Lancet Oncology, 7 (2): 119–126.Google Scholar
  22. Ouyang H L, Kong X Z, Lavoie M, He W, Qin N, He O S, Yang B, Wang R, Xu F L. 2013. Photosynthetic and cellular toxicity of cadmium in Chlorella vulgaris. Environmental Toxicology and Chemistry, 32 (12): 2 762–2 770.Google Scholar
  23. Pan X L, Zhang D Y, Chen X, Li L, Mu G J, Li L H, Bao A M, Liu J, Zhu H S, Song W J, Yang J Y, Ai J Y. 2009. Effects of short–term low temperatures on photosystem II function of samara and leaf of Siberian maple ( Acer ginnala ) and subsequent recovery. J ournal of Arid Land, 1 (1): 57–63.Google Scholar
  24. Payne C D, Price N M. 1999. Effects of cadmium toxicity on growth and elemental composition of marine phytoplankton. Journal of Phycology, 35 (2): 293–302.Google Scholar
  25. Perales–Vela H V, González–Moreno S, Montes–Horcasitas C, Cañizares–Villanueva R O. 2007. Growth, photosynthetic and respiratory responses to sub–lethal copper concentrations in Scenedesmus incrassatulus (Chlorophyceae). Chemosphere, 67 (11): 2 274–2 281.Google Scholar
  26. Perreault F, Dionne J, Didur O, Juneau P, Popovic R. 2011. Effect of cadmium on photosystem II activity in Chlamydomonas reinhardtii: alteration of O–J–I–P fluorescence transients indicating the change of apparent activation energies within photosystem II. Photosynthesis Research, 107 (2): 151–157.Google Scholar
  27. Pinto E, Sigaud–Kutner T C S, Leitão M A S, Okamoto O K, Morse D, Colepicolo P. 2003. Heavy metal–induced oxidative stress in algae. Journal of Phycology, 39 (6): 1 008–1 018.Google Scholar
  28. Pospíšil P. 2016. Production of reactive oxygen species by photosystem ii as a response to light and temperature stress. Frontiers in Plant Science, 7: 1 950.Google Scholar
  29. Rocca N L, Andreoli C, Giacometti G M, Rascio N, Moro I. 2009. Responses of the Antarctic microalga Koliella antarctica (Trebouxiophyceae, Chlorophyta) to cadmium contamination. Photosynthetica, 47 (3): 471–479.Google Scholar
  30. Ruban A V, Johnson M P, Duffy C D P. 2012. The photoprotective molecular switch in the photosystem II antenna. Biochimica et Biophysica Acta ( BBA )–Bioenergetics, 1817 (1): 167–181.Google Scholar
  31. Siedlecka A, Krupa Z. 1996. Interaction between cadmium and iron and its effects on photosynthetic capacity of primary leaves of Phaseolus vulgaris. Plant Physiology and Biochem istry, 34 (6): 833–841.Google Scholar
  32. Wang S Z, Pan X L. 2012. Effects of Sb(V) on growth and chlorophyll fluorescence of Microcystis aeruginosa (FACHB–905). Curr ent Microbiology, 65 (6): 733–741.Google Scholar
  33. Wang S Z, Zhang D Y, Pan X L. 2013. Effects of cadmium on the activities of photosystems of Chlorella pyrenoidosa and the protective role of cyclic electron flow. Chemosphere, 93 (2): 230–237.Google Scholar
  34. Yamori W, Shikanai T. 2016. Physiological functions of cyclic electron transport around photosystem i in sustaining photosynthesis and plant growth. Annual Review of Plant Biology, 67: 81–106.Google Scholar
  35. Zhang D Y, Pan X L, Mu G J, Wang J L. 2010. Toxic effects of antimony on photosystem II of Synechocystis sp. as probed by in vivo chlorophyll fluorescence. J ournal of Appl ied Phycology, 22 (4): 479–488.Google Scholar
  36. Zhao P P, Gu W H, Wu S C, Huang A Y, He L W, Xie X J, Gao S, Zhang B Y, Niu J F, Lin A P, Wang G C. 2014. Silicon enhances the growth of Phaeodactylum tricornutum Bohlin under green light and low temperature. Scientific Reports, 4: 3958.Google Scholar
  37. Zhou W B, Juneau P, Qiu B S. 2006. Growth and photosynthetic responses of the bloom–forming cyanobacterium Microcystis aeruginosa to elevated levels of cadmium. Chemosphere, 65 (10): 1 738–1 746.Google Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Yan Ji (季琰)
    • 1
  • Xiujun Xie (解修俊)
    • 2
    • 3
  • Guangce Wang (王广策)
    • 2
    • 3
    Email author
  1. 1.School of Biological and Chemical EngineeringQingdao Technical CollegeQingdaoChina
  2. 2.Key Laboratory of Experimental Marine Biology, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  3. 3.Laboratory for Marine Biology and BiotechnologyQingdao National Laboratory for Marine Science and TechnologyQingdaoChina

Personalised recommendations