Cite this paper:
JI Yan, XIE Xiujun, WANG Guangce. Effects of the heavy metal cadmium on photosynthetic activity and the xanthophyll cycle in Phaeodactylum tricornutum [J]. Journal of Oceanology and Limnology, 2018, 36(6): 2194-2201

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

JI Yan1, XIE Xiujun2,3, WANG Guangce2,3
1 School of Biological and Chemical Engineering, Qingdao Technical College, Qingdao 266555, China;
2 Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
3 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
Abstract:
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.
Key words:    heavy metal|cadmium|photosystem I|photosystem Ⅱ|Phaeodactylum tricornutum    
Received: 2017-06-09   Revised:
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References:
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.
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.
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.
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.
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.
Fargašová A, Bumbálová A, Havránek E. 1999.Ecotoxicological effects and uptake of metals (Cu+, Cu2+, Mn2+, Mo6+, Ni2+, V5+) in freshwater alga Scenedesmus quadricauda. Chemosphere, 38(5):1 165-1 173.
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.
Goss R, Lepetit B. 2015. Biodiversity of NPQ. Journal of Plant Physiology, 172:13-32.
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.
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.
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.
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.
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.
Klughammer C, Schreiber U. 2008. Saturation pulse method for assessment of energy conversion in PS I. PAM Application Notes, 1:11-14.
Kola H, Wilkinson K J. 2005. Cadmium uptake by a green alga can be predicted by equilibrium modelling. Environmental Science & Technology, 39(9):3 040-3 047.
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.
Masmoudi S, Nguyen-Deroche N, Caruso A, Ayadi H, MorantManceau 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.
Miao A J, Wang W X. 2006. Cadmium toxicity to two marine phytoplankton under different nutrient conditions. Aquatic Toxicology, 78(2):114-126.
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.
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.
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.
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.
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. Journal of Arid Land, 1(1):57-63.
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.
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.
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.
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.
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.
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.
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.
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 Biochemistry, 34(6):833-841.
Wang S Z, Pan X L. 2012. Effects of Sb(V) on growth and chlorophyll fluorescence of Microcystis aeruginosa(FACHB-905). Current Microbiology, 65(6):733-741.
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.
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.
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. Journal of Applied Phycology, 22(4):479-488.
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.
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.
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