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Shasha ZANG, Fang YAN, Daode YU, Jingjing SONG, Lei WANG, Zhiguang XU, Hongyan WU. Reduced salinity interacts with ultraviolet radiation to alter photosystem II function in diatom Skeletonema costatum[J]. Journal of Oceanology and Limnology, 2022, 40(4): 1615-1627

Reduced salinity interacts with ultraviolet radiation to alter photosystem II function in diatom Skeletonema costatum

Shasha ZANG1, Fang YAN1, Daode YU2, Jingjing SONG2, Lei WANG1,3, Zhiguang XU1,3, Hongyan WU1,3
1 College of Life Science, Ludong University, Yantai 264025, China;
2 Marine Science Research Institute of Shandong Province, Qingdao 266104, China;
3 Key Laboratory of Marine Biotechnology in Universities of Shandong(Ludong University), Yantai 264025, China
Abstract:
To investigate the effect of reduced salinity on diatoms' capacity to cope with changing ultraviolet radiation (UVR) and photosynthetically active radiation (PAR), Skeletonema costatum was grown in a range of salinity (15, 25, and 35). The photosystem II (PSII) function was analyzed by increasing PAR and UVR to mimic a mixing event in turbulent waters. The results show that high UVR exposure significantly reduced PSII activity, especially in cells grown at low salinity. UVR, but not salinity, stimulated the ‘removal’ rate of PSII protein PsbA. Salinity alone, in the range of 15 to 35, did not regulate PSII acceptor region; however, the low salinity+UVR treatment decreased the energy flux for electron transport per PSII reaction center in S. costatum. It showed that low salinity exacerbated the damaging effect of UVR on PSII function in S. costatum by suppressing PsbA protein synthesis and modifying the photochemistry of PSII. Although higher catalase (CAT) activity and NPQs were induced, they were unable to prevent the combined damage effect of low salinity+UVR. Our findings indicate that reduced salinity and increased UVR potentially affect the abundance and distribution of S. costatum with the escalation of climate disturbances.
Key words:    diatom|ultraviolet radiation (UVR)|photoinactivation|photosystem II   
Received: 2021-04-14   Revised:
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Articles by Shasha ZANG
Articles by Fang YAN
Articles by Daode YU
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Articles by Lei WANG
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Articles by Hongyan WU
References:
Allakhverdiev S I, Sakamoto A, Nishiyama Y, Inaba M, Murata N.2000.Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp.Plant Physiology, 123(3):1047-1056, https://doi.org/10.1104/pp.123.3.1047.
Ayache N, Hervé F, Lundholm N, Amzil Z, Caruana A M N.2020.Acclimation of the marine diatom Pseudo-nitzschia australis to different salinity conditions:effects on growth, photosynthetic activity, and domoic acid content.Journal of Phycology, 56(1):97-109, https://doi.org/10.1111/jpy.12929.
Bachmann K M, Ebbert V, Adams III W W, Verhoeven A S, Logan B A, Demmig-Adams B.2004.Effects of lincomycin on PSII efficiency, non-photochemical quenching, D1 protein and xanthophyll cycle during photoinhibition and recovery.Functional Plant Biology, 31(8):803-813, https://doi.org/10.1071/FP04022.
Bais A F, Bernhard G, McKenzie R L, Aucamp P J, Young P J, Ilyas M, Jöckel P, Deushi M.2019.Ozone-climate interactions and effects on solar ultraviolet radiation.Photochemical & Photobiological Sciences, 18(3):602-640, https://doi.org/10.1039/C8PP90059K.
Balzano S, Sarno D, Kooistra W H C F.2011.Effects of salinity on the growth rate and morphology of ten Skeletonema strains.Journal of Plankton Research, 33(6):937-945, https://doi.org/10.1093/plankt/fbq150.
Barnett A, Méléder V, Blommaert L, Lepetit B, Gaudin P, Vyverman W, Sabbe K, Dupuy C, Lavaud J.2015.Growth form defines physiological photoprotective capacity in intertidal benthic diatoms.The ISME Journal, 9(1):32-45, https://doi.org/10.1038/ismej.2014.105.
Bintanja R, Van Oldenborgh G J, Drijfhout S S, Wouters B, Katsman C A.2013.Important role for ocean warming and increased ice-shelf melt in Antarctic sea-ice expansion.Nature Geoscience, 6(5):376-379, https://doi.org/10.1038/ngeo1767.
Blindheim J, Borovkov V, Hansen B, Malmberg S A, Turrell W R, Østerhus S.2000.Upper layer cooling and freshening in the Norwegian Sea in relation to atmospheric forcing.Deep Sea Research Part I:Oceanographic Research Papers, 47(4):655-680, https://doi.org/10.1016/S0967-0637(99)00070-9.
Boller A J, Thomas P J, Cavanaugh C M, Scott K M.2015.Isotopic discrimination and kinetic parameters of RubisCO from the marine bloom-forming diatom, Skeletonema costatum.Geobiology, 13(1):33-43, https://doi.org/10.1111/gbi.12112.
Brown C M, MacKinnon J D, Cockshutt A M, Villareal T A, Campbell D A.2008.Flux capacities and acclimation costs in Trichodesmium from the Gulf of Mexico.Marine Biology, 154(3):413-422, https://doi.org/10.1007/s00227-008-0933-z.
Bussard A, Corre E, Hubas C, Duvernois-Berthet E, Corguillé G L, Jourdren L, Coulpier F, Claquin P, Lopez P J.2017.Physiological adjustments and transcriptome reprogramming are involved in the acclimation to salinity gradients in diatoms.Environmental Microbiology, 19:909-925, http://doi:10.1111/1462-2920.13398.
Campbell D A, Tyystjärvi E.2012.Parameterization of photosystem II photoinactivation and repair.Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1817(1):258-265, https://doi.org/10.1016/j.bbabio.2011.04.010.
Eaton-Rye J J, Sobotka R.2017.Editorial:assembly of the photosystem II membrane-protein complex of oxygenic photosynthesis.Frontiers in Plant Science, 8:884, https://doi.org/10.3389/fpls.2017.00884.
Edelman M, Mattoo A K.2008.D1-protein dynamics in photosystem II:the lingering enigma.Photosynthesis Research, 98(1):609-620, https://doi.org/10.1007/s11120-008-9342-x.
Falkowski P.2012.Ocean science:the power of plankton.Nature, 483(7387):S17-S20, https://doi.org/10.1038/483S17a.
Gao G, Gao K S, Giordano M.2009.Responses to solar UV radiation of the diatom Skeletonema costatum(Bacillariophyceae) grown at different Zn2+ concentrations.Journal of Phycology, 45(1):119-129, https://doi.org/10.1111/j.1529-8817.2008.00616.x.
Gao G, Qu L M, Xu T P, Burgess J G, Li X S, Xu J T.2019.Future CO2-induced ocean acidification enhances resilience of a green tide alga to low-salinity stress.ICES Journal of Marine Science, 76(7):2437-2445, https://doi.org/10.1093/icesjms/fsz135.
Gao G, Shi Q, Xu Z G, Xu J T, Campbell D A, Wu H Y.2018.Global warming interacts with ocean acidification to alter PSII function and protection in the diatom Thalassiosira weissflogii.Environmental and Experimental Botany, 147:95-103, https://doi.org/10.1016/j.envexpbot.2017.11.014.
Gattuso J P, Magnan A, Billé R, Cheung W W L, Howes E L, Joos F, Allemand D, Bopp L, Cooley S R, Eakin C M, Hoegh-Guldberg O, Kelly R P, Pörtner H O, Rogers A D, Baxter J M, Laffoley D, Osborn D, Rankovic A, Rochette J, Sumaila U R, Treyer S, Turley C.2015.Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios.Science, 349(6243):aac4722, https://doi.org/10.1126/science.aac4722.
Goss R, Jakob T.2010.Regulation and function of xanthophyll cycle-dependent photoprotection in algae.Photosynthesis Research, 106(1):103-122, https://doi.org/10.1007/s11120-010-9536-x.
Goss R, Mewes H, Wilhelm C.1999.Stimulation of the diadinoxanthin cycle by UV-B radiation in the diatom Phaeodactylum tricornutum.Photosynthesis Research, 59(1):73-80, https://doi.org/10.1023/A:1006169901482.
Guillard R R L, Ryther J H.1962.Studies of marine planktonic diatoms:I.Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran.Canadian Journal of Microbiology, 8(2):229-239, https://doi.org/10.1139/m62-029.
Häder D P, Gao K S.2017.The impacts of climate change on marine phytoplankton.In:Phillips B F, Pérez-Ramírez M eds.Climate Change Impacts on Fisheries and Aquaculture:A Global Analysis, I.John Wiley & Sons Ltd, Hoboken.p.897-924.
Häder D P, Kumar H D, Smith R C, Worrest R C.2007.Effects of solar UV radiation on aquatic ecosystems and interactions with climate change.Photochemical & Photobiological Sciences, 6(3):267-285, https://doi.org/10.1039/B700020K.
Häder D P, Williamson C E, Wängberg S Å, Rautio M, Rose K C, Gao K S, Helbling E W, Sinha R P, Worrest R.2015.Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors.Photochemical & Photobiological Sciences, 14(1):108-126, https://doi.org/10.1039/C4PP90035A.
Halac S R, Villafañe V E, Helbling E W.2010.Temperature benefits the photosynthetic performance of the diatoms Chaetoceros gracilis and Thalassiosira weissflogii when exposed to UVR.Journal of Photochemistry and Photobiology B:Biology, 101(3):196-205, https://doi.org/10.1016/j.jphotobiol.2010.07.003.
Harrison J W, Smith R E H.2009.Effects of ultraviolet radiation on the productivity and composition of freshwater phytoplankton communities.Photochemical & Photobiological Sciences, 8(9):1218-1232, https://doi.org/10.1039/b902604e.
Helbling E W, Buma A G J, Boelen P, Van Der Strate H J, Giordanino M V F, Villafañe V E.2011.Increase in Rubisco activity and gene expression due to elevated temperature partially counteracts ultraviolet radiationinduced photoinhibition in the marine diatom Thalassiosira weissflogii.Limnology and Oceanography, 56(4):1330-1342, https://doi.org/10.4319/lo.2011.56.4.1330.
Intergovernmental Panel on Climate Change.2013.The physical science basis.In:Stocker T F, Qin D, Plattner G K, Tignor M M B, Allen S K, Boschung J, Nauels A, Xia Y, Bex V, Midgley P M eds.Climate change 2013:Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.Cambridge University Press, Cambridge.p.6-10.
Jiang H B, Qiu B S.2005.Photosynthetic adaptation of a bloom-forming cyanobacterium Microcystis aeruginosa(Cyanophyceae) to prolonged UV-B exposure.Journal of Phycology, 41(5):983-992, https://doi.org/10.1111/j.1529-8817.2005.00126.x.
Jin P, Gao K S, Villafañe V E, Campbell D A, Helbling E W.2013.Ocean acidification alters the photosynthetic responses of a coccolithophorid to fluctuating ultraviolet and visible radiation.Plant Physiology, 162(4):2084-2094, https://doi.org/10.1104/pp.113.219543.
Kamenos N A, Hoey T B, Nienow P, Fallick A E, Claverie T.2012.Reconstructing Greenland ice sheet runoff using coralline algae.Geology, 40:1095-1098, https://doi.org/10.1130/G33405.1.
Kang E J, Kim J H, Kim K, Kim K Y.2016.Adaptations of a green tide forming Ulva linza (Ulvophyceae, Chlorophyta) to selected salinity and nutrients conditions mimicking representative environments in the Yellow Sea.Phycologia, 55(2):210-218, https://doi.org/10.2216/15-67.1.
Kirrolia A, Bishnoi N R, Singh N.2011.Salinity as a factor affecting the physiological and biochemical traits of Scenedesmus quadricauda.Journal of Algal Biomass Utilization, 2(4):28-34.
Kok B.1956.On the inhibition of photosynthesis by intense light.Biochimica et Biophysica Acta, 21(2):234-244, https://doi.org/10.1016/0006-3002(56)90003-8.
Komenda J, Sobotka R, Nixon P J.2012.Assembling and maintaining the Photosystem II complex in chloroplasts and cyanobacteria.Current Opinion in Plant Biology, 15(3):245-251, https://doi.org/10.1016/j.pbi.2012.01.017.
Kooistra W H C F, Sarno D, Balzano S, Gu H F, Andersen R A, Zingone A.2008.Global diversity and biogeography of Skeletonema species (Bacillariophyta).Protist, 159(2):177-193, https://doi.org/10.1016/j.protis.2007.09.004.
Lavaud J, Goss R.2014.The peculiar features of nonphotochemical fluorescence quenching in diatoms and brown algae.In:Demmig-Adams B, Garab G, Adams III W, Govindjee eds.Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria.springer, Dordrecht.p.421-443.
Lavaud J, Lepetit B.2013.An explanation for the interspecies variability of the photoprotective nonphotochemical chlorophyll fluorescence quenching in diatoms.Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1827(3):294-302, https://doi.org/10.1016/j.bbabio.2012.11.012.
Lavaud J, Rousseau B, Etienne A L.2004.General features of photoprotection by energy dissipation in planktonic diatoms(Bacillariophyceae).Journal of Phycology, 40:130-137, https://doi.org/10.1046/j.1529-8817.2004.03026.x.
Li W, Gao K, Beardall J.2015.Nitrate limitation and ocean acidification interact with UV-B to reduce photosynthetic performance in the diatom Phaeodactylum tricornutum.Biogeosciences, 12(8):2383-2393, https://doi.org/10.5194/bg-12-2383-2015.
MacIntyre H L, Kana T M, Geider R J.2000.The effect of water motion on short-term rates of photosynthesis by marine phytoplankton.Trends in Plant Science, 5(1):12-17, https://doi.org/10.1016/S1360-1385(99)01504-6.
Markina Z V, Aizdaicher N A.2016.The effect of lowered salinity of sea water on the growth and photosynthetic pigment content in three strains of the microalgae Pseudo-nitzschia pungens (Grunow ex.P.T.Cleve)Hasle, 1993 (Bacillariophyta).Russian Journal of Marine Biology, 42(5):414-418, https://doi.org/10.1134/s1063074016050060.
Neale P J, Thomas B C.2017.Inhibition by ultraviolet and photosynthetically available radiation lowers model estimates of depth-integrated picophytoplankton photosynthesis:global predictions for Prochlorococcus and Synechococcus.Global Chang Biology, 23(1):293-306, https://doi.org/10.1111/gcb.13356.
Nishiyama Y, Allakhverdiev S I, Murata N.2006.A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II.Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1757(7):742-749, https://doi.org/10.1016/j.bbabio.2006.05.013.
Nishiyama Y, Murata N.2014.Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery.Applied Microbiology and Biotechnology, 98(21):8777-8796, https://doi.org/10.1007/s00253-014-6020-0.
Nixon P J, Michoux F, Yu J F, Boehm M, Komenda J.2010.Recent advances in understanding the assembly and repair of photosystem II.Annals of Botany, 106(1):1-16, https://doi.org/10.1093/aob/mcq059.
Pawlowicz R.2015.The Absolute Salinity of seawater diluted by riverwater.Deep Sea Research Part I:Oceanographic Research Papers, 101:71-79, https://doi.org/10.1016/j.dsr.2015.03.006.
Pelah D, Sintov A, Cohen E.2004.The effect of salt stress on the production of canthaxanthin and astaxanthin by Chlorella zofingiensis grown under limited light intensity.World Journal of Microbiology and Biotechnology, 20(5):483-486, https://doi.org/10.1023/B:WIBI.0000040398.93103.21.
Pugkaew W, Meetam M, Yokthongwattana K, Leeratsuwan N, Pokethitiyook P.2019.Effects of salinity changes on growth, photosynthetic activity, biochemical composition, and lipid productivity of marine microalga Tetraselmis suecica.Journal of Applied Phycology, 31(2):969-979, https://doi.org/10.1007/s10811-018-1619-7.
Radchenko I G, Il'yash L V.2006.Growth and photosynthetic activity of diatom Thalassiosira weissflogii at decreasing salinity.Biology Bulletin, 33(3):242-247, https://doi.org/10.1134/S106235900603006X.
Rai S V, Rajashekhar M.2014.Effect of pH, salinity and temperature on the growth of six species of marine phytoplankton.Journal of Algal Biomass Utilization,5(4):55-59.
Rijstenbil J W.2005.UV-and salinity-induced oxidative effects in the marine diatom Cylindrotheca closterium during simulated emersion.Marine Biology, 147(5):1063-1073, https://doi.org/10.1007/s00227-005-0015-4.
Rückamp M, Braun M, Suckro S, Blindow N.2011.Observed glacial changes on the King George Island ice cap, Antarctica, in the last decade.Global and Planetary Change, 79(1-2):99-109, https://doi.org/10.1016/j.gloplacha.2011.06.009.screen J A, Simmonds I.2010.The central role of diminishing sea ice in recent Arctic temperature amplification.Nature, 464(7293):1334-1337, https://doi.org/10.1038/nature09051.
Shiu C T, Lee T M.2005.Ultraviolet-B-induced oxidative stress and responses of the ascorbate-glutathione cycle in a marine macroalga Ulva fasciata.Journal of Experimental Botany, 56(421):2851-2865, https://doi.org/10.1093/jxb/eri277.
Silva P, Thompson E, Bailey S, Kruse O, Mullineaux C W, Robinson C, Mann N H, Nixon P J.2003.FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803.The Plant Cell, 15(9):2152-2164, https://doi.org/10.1105/tpc.012609.
Sobrino C, Neale P J, Montero O, Lubián L M.2005.Biological weighting function for xanthophyll de-epoxidation induced by ultraviolet radiation.Physiologia Plantarum, 125(1):41-51, https://doi.org/10.1111/j.1399-3054.2005.00538.x.
Strasser R J, Srivastava A, Tsimilli-Michael M.2000.The fluorescence transient as a tool to characterize and screen photosynthetic samples.In:Yunus M, Pathre U, Mohanty P eds.Probing Photosynthesis:Mechanism, Regulation & Adaptation.Taylor and Francis, London.p.443-480.
Thorpe L, Andrews T.2014.The physical drivers of historical and 21st century global precipitation changes.Environmental Research Letters, 9(6):064024, https://doi.org/10.1088/1748-9326/9/6/064024.
Trenberth K E, Jones P D.2007.Observations:surface and atmospheric climate change.In:Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt K B, Tignor M, Miller H L eds.Climate Change 2007:The Physical Science Basis:Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.Cambridge University Press, Cambridge.p.235-336.
Tyystjärvi E, Aro E M.1996.The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity.Proceedings of the National Academy of Sciences of the United States of America, 93(5):2213-2218, https://doi.org/10.1073/pnas.93.5.2213.
Vartanian M, Desclés J, Quinet M, Douady S, Lopez P J.2009.Plasticity and robustness of pattern formation in the model diatom Phaeodactylum tricornutum.New Phytologist, 182(2):429-442, https://doi.org/10.1111/j.1469-8137.2009.02769.x.
Vass I, Kirilovsky D, Etienne A L.1999.UV-B radiationinduced donor-and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp.PCC 6803.Biochemistry, 38(39):12786-12794, https://doi.org/10.1021/bi991094w.
Wang M H, Wang G Z.2010.Oxidative damage effects in the copepod Tigriopus japonicus Mori experimentally exposed to nickel.Ecotoxicology, 19(2):273-284, https://doi.org/10.1007/s10646-009-0410-6.
Williamson C E, Neale P J, Hylander S, Rose K C, Figueroa F L, Robinson S A, Häder D P, Wängberg S Å, Worrest R C.2019.The interactive effects of stratospheric ozone depletion, UV radiation, and climate change on aquatic ecosystems.Photochemical & Photobiological Sciences, 18(3):717-746, https://doi.org/10.1039/C8PP90062K.
Wu H Y, Cockshutt A M, McCarthy A, Campbell D A.2011.Distinctive photosystem II photoinactivation and protein dynamics in marine diatoms.Plant Physiology, 156(4):2184-2195, https://doi.org/10.1104/pp.111.178772.
Wu H Y, Roy S, Alami M, Green B R, Campbell D A.2012.Photosystem II photoinactivation, repair, and protection in marine centric diatoms.Plant Physiology, 160(1):464-476, https://doi.org/10.1104/pp.112.203067.
Wu Y P, Zhu Y C, Xu J T.2017.High salinity and UVR synergistically reduce the photosynthetic performance of an intertidal benthic diatom.Marine Environmental Research, 130:258-263, https://doi.org/10.1016/j.marenvres.2017.08.004.
Xu J K, Sun J Z, Beardall J, Gao K S.2020.Lower salinity leads to improved physiological performance in the Coccolithophorid Emiliania huxleyi, which partly ameliorates the effects of ocean acidification.Frontiers in Marine Science, 7:704, https://doi.org/10.3389/fmars.2020.00704.
Yan T, Zhou M J, Qian P Y.2002.Combined effects of temperature, irradiance and salinity on growth of diatom Skeletonema costatum.Chinese Journal of Oceanology and Limnology, 20(3):237-243, https://doi.org/10.1007/BF02848852.
Young J N, Morel F M M.2015.Biological oceanography:the CO2 switch in diatoms.Nature Climate Change, 5(8):722-723, https://doi.org/10.1038/nclimate2691.
Yuan W B, Gao G, Shi Q, Xu Z G, Wu H Y.2018.Combined effects of ocean acidification and warming on physiological response of the diatom Thalassiosira pseudonana to light challenges.Marine Environmental Research, 135:63-69, https://doi.org/10.1016/j.marenvres.2018.01.016.
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