Fast acclimation of phytoplankton assemblies to acute salinity stress in the Jiulong River Estuary
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摘要
Mixing of freshwater and seawater creates the well-known salinity gradients along the estuaries. In order to investigate how phytoplankton respond to the acute salinity changes, we exposed natural phytoplankton assemblies from the Jiulong River Estuary to differential saline field water while continuously monitoring their photosynthetic performances under both indoor-and outdoor-growth conditions. When the natural cell assemblies from salinity 30 field water were exposed to series low saline field water(salinity 25, 17, 13 and 7.5), the effective Photosystem II quantum yield(ΔF/F_m′) decreased sharply, e.g., to one-fifth of its initials after 5 min exposure to salinity 7.5 field water, and then increased fast during the following 40 min and almost completely recovered after 320 min. During such an exposure process, non-photochemical quenching(NPQ) sharply increased from 0 to 0.85 within 5 min, and then decreased to nearly 0 within the following 70 min. When these cells re-acclimated to salinity 7.5 field water were exposed to series high saline field water(salinity 13, 17, 25 and 30), a similar response pattern was observed, with the decreased ΔF/F_m′ accompanied with increased NPQ, and followed by the recovery-induced increase in ΔF/F_m′ and decrease in NPQ. A similar response pattern as ΔF/F_m′to the acute osmotic stress was also observed in the photosynthetic carbon fixation capacity according to radiocarbon(~(14)C) incorporation. Our results indicate that estuarine phytoplankton assemblies could rapidly recover from the acute osmotic stress, implying a potential cause for their frequent blooms in coastal-estuarine waters where despite drastically varying salinity, available nutrients are abundant due to the land-derived runoffs or mixing-caused relaxations from sediments.
Mixing of freshwater and seawater creates the well-known salinity gradients along the estuaries. In order to investigate how phytoplankton respond to the acute salinity changes, we exposed natural phytoplankton assemblies from the Jiulong River Estuary to differential saline field water while continuously monitoring their photosynthetic performances under both indoor-and outdoor-growth conditions. When the natural cell assemblies from salinity 30 field water were exposed to series low saline field water(salinity 25, 17, 13 and 7.5), the effective Photosystem II quantum yield(ΔF/F_m′) decreased sharply, e.g., to one-fifth of its initials after 5 min exposure to salinity 7.5 field water, and then increased fast during the following 40 min and almost completely recovered after 320 min. During such an exposure process, non-photochemical quenching(NPQ) sharply increased from 0 to 0.85 within 5 min, and then decreased to nearly 0 within the following 70 min. When these cells re-acclimated to salinity 7.5 field water were exposed to series high saline field water(salinity 13, 17, 25 and 30), a similar response pattern was observed, with the decreased ΔF/F_m′ accompanied with increased NPQ, and followed by the recovery-induced increase in ΔF/F_m′ and decrease in NPQ. A similar response pattern as ΔF/F_m′to the acute osmotic stress was also observed in the photosynthetic carbon fixation capacity according to radiocarbon(~(14)C) incorporation. Our results indicate that estuarine phytoplankton assemblies could rapidly recover from the acute osmotic stress, implying a potential cause for their frequent blooms in coastal-estuarine waters where despite drastically varying salinity, available nutrients are abundant due to the land-derived runoffs or mixing-caused relaxations from sediments.
Mixing of freshwater and seawater creates the well-known salinity gradients along the estuaries. In order to investigate how phytoplankton respond to the acute salinity changes, we exposed natural phytoplankton assemblies from the Jiulong River Estuary to differential saline field water while continuously monitoring their photosynthetic performances under both indoor-and outdoor-growth conditions. When the natural cell assemblies from salinity 30 field water were exposed to series low saline field water(salinity 25, 17, 13 and 7.5), the effective Photosystem II quantum yield(ΔF/F_m′) decreased sharply, e.g., to one-fifth of its initials after 5 min exposure to salinity 7.5 field water, and then increased fast during the following 40 min and almost completely recovered after 320 min. During such an exposure process, non-photochemical quenching(NPQ) sharply increased from 0 to 0.85 within 5 min, and then decreased to nearly 0 within the following 70 min. When these cells re-acclimated to salinity 7.5 field water were exposed to series high saline field water(salinity 13, 17, 25 and 30), a similar response pattern was observed, with the decreased ΔF/F_m′ accompanied with increased NPQ, and followed by the recovery-induced increase in ΔF/F_m′ and decrease in NPQ. A similar response pattern as ΔF/F_m′to the acute osmotic stress was also observed in the photosynthetic carbon fixation capacity according to radiocarbon(~(14)C) incorporation. Our results indicate that estuarine phytoplankton assemblies could rapidly recover from the acute osmotic stress, implying a potential cause for their frequent blooms in coastal-estuarine waters where despite drastically varying salinity, available nutrients are abundant due to the land-derived runoffs or mixing-caused relaxations from sediments.
引文
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Cao Wenzhi,Huang Zheng,Zhai Weidong,et al.2015.Isotopic evidence on multiple sources of nitrogen in the northern Jiulong River,Southeast China.Estuarine,Coastal and Shelf Science,163:37-43,doi:10.1016/j.ecss.2015.05.042
Chen Baohong,Chen Changping,Chen Jinmin,et al.2012.Variations of nutrient content and ratios and their impact on phytoplankton community in Xiamen waters.Journal of Oceanography in Taiwan Strait(in Chinese),31(2):246-253
Chen Baohong,Ji Weidong,Chen Jinmin,et al.2013a.Characteristics of nutrients in the Jiulong River and its impact on Xiamen Water,China.Chinese Journal of Oceanology and Limnology,31(5):1055-1063,doi:10.1007/s00343-013-2263-3
Chen Nengwang,Peng Benrong,Hong Huasheng,et al.2013b.Nutrient enrichment and N:P ratio decline in a coastal bay-river system in southeast China:The need for a dual nutrient(N and P)management strategy.Ocean&Coastal Management,81:7-13
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D'ors A,BartoloméM C,Sánchez-Fortún S.2016.Repercussions of salinity changes and osmotic stress in marine phytoplankton species.Estuarine,Coastal and Shelf Science,175:169-175,doi:10.1016/j.ecss.2016.04.004
Doucette G J,King K L,Thessen A E,et al.2008.The effect of salinity on domoic acid production by the diatom Pseudo-Nitzschia multiseries.Nova Hedwigia Beiheft,133:31-46
Finkel Z V,Beardall J,Flynn K J,et al.2010.Phytoplankton in a changing world:cell size and elemental stoichiometry.Journal of Plankton Research,32(1):119-137,doi:10.1093/plankt/fbp098
Gao Guang,Xia Jianrong,Yu Jinlan,et al.2018.Physiological response of a red tide alga(Skeletonema costatum)to nitrate enrichment,with special reference to inorganic carbon acquisition.Marine Environmental Research,133:15-23,doi:10.1016/j.marenvres.2017.11.003
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H?ubner N,Sylvander P,Vuori K,et al.2014.Abiotic stress modifies the synthesis of alpha-tocopherol and beta-carotene in phytoplankton species.Journal of Phycology,50(4):753-759,doi:10.1111/jpy.2014.50.issue-4
Hernando M,Schloss I R,Malanga G,et al.2015.Effects of salinity changes on coastal Antarctic phytoplankton physiology and assemblage composition.Journal of Experimental Marine Biology and Ecology,466:110-119,doi:10.1016/j.jembe.2015.02.012
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Huang Xuguang,Guo Donghui,Xiao Wupeng,et al.2012.The relationship between quantitative changes of microplankton and population dynamics of small medusa in the Jiulong River estuary in spring of 2011.Oceanologia et Limnologia Sinica(in Chinese),43(3):579-583
Huang Liangmin,Jian Weijun,Song Xingyu,et al.2004.Species diversity and distribution for phytoplankton of the Pearl River estuary during rainy and dry seasons.Marine Pollution Bulletin,49(7-8):588-596,doi:10.1016/j.marpolbul.2004.03.015
Li Ying,Cao Wenzhi,Su Caixia,et al.2011a.Nutrient sources and composition of recent algal blooms and eutrophication in the northern Jiulong River,Southeast China.Marine Pollution Bulletin,63(5-12):249-254,doi:10.1016/j.marpolbul.2011.02.021
Li Gang,Gao Kunshan,Yuan Dongxing,et al.2011b.Relationship of photosynthetic carbon fixation with environmental changes in the Jiulong River estuary of the South China Sea,with special reference to the effects of solar UV radiation.Marine Pollution Bulletin,62(8):1852-1858,doi:10.1016/j.marpolbul.2011.02.050
Li Gang,Lin Qiang,Lin Junda,et al.2014.Environmental gradients regulate the spatial variations of phytoplankton biomass and community structure in surface water of the Pearl River estuary.Acta Ecologica Sinica,34(2):129-133,doi:10.1016/j.chnaes.2014.01.002
Licursi M,Sierra M V,Gómez N.2006.Diatom assemblages from a turbid coastal plain estuary:Río de la Plata(South America).Journal of Marine Systems,62(1-2):35-45,doi:10.1016/j.jmarsys.2006.03.002
Lim P T,Ogata T.2005.Salinity effect on growth and toxin production of four tropical Alexandrium species(Dinophyceae).Toxicon,45(6):699-710,doi:10.1016/j.toxicon.2005.01.007
Liu Guangping,Hu Jianyu,Chen Zhaozhang,et al.2008.Distribution characteristics of sea surface salinity and its relations to tide in Jiulongjiang estuary-Xiamen Bay.Journal of Xiamen University(Natural Science)(in Chinese),47(5):710-713
Liu Lemian,Yang Jun,Yu Xiaoqing,et al.2013.Patterns in the composition of microbial communities from a subtropical river:effects of environmental,spatial and temporal factors.PLoS One,8(11):e81232,doi:10.1371/journal.pone.0081232
Lu Chongming,Zhang Jianhua.1999.Effects of salt stress on PSIIfunction and photoinhibition in the cyanobacterium Spirulina platensis.Journal of Plant Physiology,155(6):740-745,doi:10.1016/S0176-1617(99)80091-1
Mo Yu,Lin Lizhen,Zheng Liping,et al.2013.Phytoplankton phosphorus stress of Jiulongjiang River-Estuary and adjacent waters system in summer.Oceanologia et Limnologia Sinica(in Chinese),44(1):241-248
Murphy J,Riley J P.1962.A modified single solution method for the determination of phosphate in natural waters.Analytica Chimica Acta,27:31-36,doi:10.1016/S0003-2670(00)88444-5
Muylaert K,Sabbe K,Vyverman W.2009.Changes in phytoplankton diversity and community composition along the salinity gradient of the Schelde estuary(Belgium/The Netherlands).Estuarine,Coastal and Shelf Science,82(2):335-340,doi:10.1016/j.ecss.2009.01.024
Nche-Fambo F A,Scharler U M,Tirok K.2015.Resilience of estuarine phytoplankton and their temporal variability along salinity gradients during drought and hypersalinity.Estuarine,Coastal and Shelf Science,158:40-52,doi:10.1016/j.ecss.2015.03.011
Pai Sucheng,Tsau Y J,Yang T I.2001.pH and buffering capacity problems involved in the determination of ammonia in saline water using the indophenol blue spectrophotometric method.Analytica Chimica Acta,434(2):209-216,doi:10.1016/S0003-2670(01)00851-0
Porra R J.2002.The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b.Photosynthesis Research,73(1-3):149-156
Radchenko I G,Il’iash L V.2006.Growth and photosynthetic activity of diatom Thalassiosira weissflogii at decreasing salinity.Izvestiia Akademii Nauk.Seriia Biologicheskaia,(3):306-313
Raven J A.1998.The twelfth tansley lecture,small is beautiful:the picophytoplankton.Functional Ecology,12(4):503-513,doi:10.1046/j.1365-2435.1998.00233.x
Rijstenbil J W,Mur L R,Wijnholds J J,et al.1989a.Impact of a temporal salinity decrease on growth and nitrogen metabolism of the marine diatom Skeletonema costatum in continuous cultures.Marine Biology,101(1):121-129,doi:10.1007/BF00393485
Rijstenbil J W,Wijnholds J A,Sinke J J.1989b.Implications of salinity fluctuation for growth and nitrogen metabolism of the marine diatom Ditylum brightwellii in comparison with Skeletonema costatum.Marine Biology,101(1):131-141,doi:10.1007/BF00393486
Tang Rongkun,He Qing,Ji Weidong,et al.2010.Characteristics of temporal and spatial variations in chlorophyll contents of waters around Xiamen Island in 2005~2007.Journal of Oceanography in Taiwan Strait(in Chinese),29(3):342-351
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Armstrong F A J,Stearns C R,Strickland J D H.1967.The measurement of upwelling and subsequent biological process by means of the Technicon Autoanalyzer?and associated equipment.Deep Sea Research and Oceanographic Abstracts,14(3):381-389,doi:10.1016/0011-7471(67)90082-4
Brand L E.1984.The salinity tolerance of forty-six marine phytoplankton isolates.Estuarine,Coastal and Shelf Science,18(5):543-556,doi:10.1016/0272-7714(84)90089-1
Cai Aizhi,Cai Yuee,Zhu Xiaoning,et al.1991.Diffusion and modern sedimentation of seaward-transporting discharges in the estuary of Jiulongjiang River,Fujian Province.Marine Geology&Quaternary Geology(in Chinese),11(1):57-67
Cao Zhenrui,Huang Bangqin,Liu Yuan,et al.2005.Distribution characteristics of size-fractionated chlorophyll a in Xiamen waters.Journal of Oceanography in Taiwan Strait(in Chinese),24(4):493-501
Cao Wenzhi,Huang Zheng,Zhai Weidong,et al.2015.Isotopic evidence on multiple sources of nitrogen in the northern Jiulong River,Southeast China.Estuarine,Coastal and Shelf Science,163:37-43,doi:10.1016/j.ecss.2015.05.042
Chen Baohong,Chen Changping,Chen Jinmin,et al.2012.Variations of nutrient content and ratios and their impact on phytoplankton community in Xiamen waters.Journal of Oceanography in Taiwan Strait(in Chinese),31(2):246-253
Chen Baohong,Ji Weidong,Chen Jinmin,et al.2013a.Characteristics of nutrients in the Jiulong River and its impact on Xiamen Water,China.Chinese Journal of Oceanology and Limnology,31(5):1055-1063,doi:10.1007/s00343-013-2263-3
Chen Nengwang,Peng Benrong,Hong Huasheng,et al.2013b.Nutrient enrichment and N:P ratio decline in a coastal bay-river system in southeast China:The need for a dual nutrient(N and P)management strategy.Ocean&Coastal Management,81:7-13
Cloern J E.1999.The relative importance of light and nutrient limitation of phytoplankton growth:a simple index of coastal ecosystem sensitivity to nutrient enrichment.Aquatic Ecology,33(1):3-15,doi:10.1023/A:1009952125558
Domingues R B,Anselmo T P,Barbosa A B,et al.2010.Tidal variability of phytoplankton and environmental drivers in the freshwater reaches of the Guadiana Estuary(SW Iberia).International Review of Hydrobiology,95(4-5):352-369,doi:10.1002/iroh.v95:4/5
D'ors A,BartoloméM C,Sánchez-Fortún S.2016.Repercussions of salinity changes and osmotic stress in marine phytoplankton species.Estuarine,Coastal and Shelf Science,175:169-175,doi:10.1016/j.ecss.2016.04.004
Doucette G J,King K L,Thessen A E,et al.2008.The effect of salinity on domoic acid production by the diatom Pseudo-Nitzschia multiseries.Nova Hedwigia Beiheft,133:31-46
Finkel Z V,Beardall J,Flynn K J,et al.2010.Phytoplankton in a changing world:cell size and elemental stoichiometry.Journal of Plankton Research,32(1):119-137,doi:10.1093/plankt/fbp098
Gao Guang,Xia Jianrong,Yu Jinlan,et al.2018.Physiological response of a red tide alga(Skeletonema costatum)to nitrate enrichment,with special reference to inorganic carbon acquisition.Marine Environmental Research,133:15-23,doi:10.1016/j.marenvres.2017.11.003
Genty B,Briantais J M,Baker N R.1989.The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.Biochimica et Biophysica Acta(BBA)-General Subjects,990(1):87-92,doi:10.1016/S0304-4165(89)80016-9
Giacobbe M G,Oliva F D,Maimone G.1996.Environmental factors and seasonal occurrence of the dinoflagellate Alexandrium minutum,a PSP potential producer,in a Mediterranean lagoon.Estuarine,Coastal and Shelf Science,42(5):539-549,doi:10.1006/ecss.1996.0035
H?ubner N,Sylvander P,Vuori K,et al.2014.Abiotic stress modifies the synthesis of alpha-tocopherol and beta-carotene in phytoplankton species.Journal of Phycology,50(4):753-759,doi:10.1111/jpy.2014.50.issue-4
Hernando M,Schloss I R,Malanga G,et al.2015.Effects of salinity changes on coastal Antarctic phytoplankton physiology and assemblage composition.Journal of Experimental Marine Biology and Ecology,466:110-119,doi:10.1016/j.jembe.2015.02.012
Holm-Hansen O,Helbling E W.1995.Técnicas para la medición de la productividad primaria en el fitoplancton.In:Alveal K,Ferrario M E,Oliveira E C,et al,eds.Manual de Métodos Ficoló-gicos.Concepción:Universidad de Concepción,329-350
Huang Xuguang,Guo Donghui,Xiao Wupeng,et al.2012.The relationship between quantitative changes of microplankton and population dynamics of small medusa in the Jiulong River estuary in spring of 2011.Oceanologia et Limnologia Sinica(in Chinese),43(3):579-583
Huang Liangmin,Jian Weijun,Song Xingyu,et al.2004.Species diversity and distribution for phytoplankton of the Pearl River estuary during rainy and dry seasons.Marine Pollution Bulletin,49(7-8):588-596,doi:10.1016/j.marpolbul.2004.03.015
Li Ying,Cao Wenzhi,Su Caixia,et al.2011a.Nutrient sources and composition of recent algal blooms and eutrophication in the northern Jiulong River,Southeast China.Marine Pollution Bulletin,63(5-12):249-254,doi:10.1016/j.marpolbul.2011.02.021
Li Gang,Gao Kunshan,Yuan Dongxing,et al.2011b.Relationship of photosynthetic carbon fixation with environmental changes in the Jiulong River estuary of the South China Sea,with special reference to the effects of solar UV radiation.Marine Pollution Bulletin,62(8):1852-1858,doi:10.1016/j.marpolbul.2011.02.050
Li Gang,Lin Qiang,Lin Junda,et al.2014.Environmental gradients regulate the spatial variations of phytoplankton biomass and community structure in surface water of the Pearl River estuary.Acta Ecologica Sinica,34(2):129-133,doi:10.1016/j.chnaes.2014.01.002
Licursi M,Sierra M V,Gómez N.2006.Diatom assemblages from a turbid coastal plain estuary:Río de la Plata(South America).Journal of Marine Systems,62(1-2):35-45,doi:10.1016/j.jmarsys.2006.03.002
Lim P T,Ogata T.2005.Salinity effect on growth and toxin production of four tropical Alexandrium species(Dinophyceae).Toxicon,45(6):699-710,doi:10.1016/j.toxicon.2005.01.007
Liu Guangping,Hu Jianyu,Chen Zhaozhang,et al.2008.Distribution characteristics of sea surface salinity and its relations to tide in Jiulongjiang estuary-Xiamen Bay.Journal of Xiamen University(Natural Science)(in Chinese),47(5):710-713
Liu Lemian,Yang Jun,Yu Xiaoqing,et al.2013.Patterns in the composition of microbial communities from a subtropical river:effects of environmental,spatial and temporal factors.PLoS One,8(11):e81232,doi:10.1371/journal.pone.0081232
Lu Chongming,Zhang Jianhua.1999.Effects of salt stress on PSIIfunction and photoinhibition in the cyanobacterium Spirulina platensis.Journal of Plant Physiology,155(6):740-745,doi:10.1016/S0176-1617(99)80091-1
Mo Yu,Lin Lizhen,Zheng Liping,et al.2013.Phytoplankton phosphorus stress of Jiulongjiang River-Estuary and adjacent waters system in summer.Oceanologia et Limnologia Sinica(in Chinese),44(1):241-248
Murphy J,Riley J P.1962.A modified single solution method for the determination of phosphate in natural waters.Analytica Chimica Acta,27:31-36,doi:10.1016/S0003-2670(00)88444-5
Muylaert K,Sabbe K,Vyverman W.2009.Changes in phytoplankton diversity and community composition along the salinity gradient of the Schelde estuary(Belgium/The Netherlands).Estuarine,Coastal and Shelf Science,82(2):335-340,doi:10.1016/j.ecss.2009.01.024
Nche-Fambo F A,Scharler U M,Tirok K.2015.Resilience of estuarine phytoplankton and their temporal variability along salinity gradients during drought and hypersalinity.Estuarine,Coastal and Shelf Science,158:40-52,doi:10.1016/j.ecss.2015.03.011
Pai Sucheng,Tsau Y J,Yang T I.2001.pH and buffering capacity problems involved in the determination of ammonia in saline water using the indophenol blue spectrophotometric method.Analytica Chimica Acta,434(2):209-216,doi:10.1016/S0003-2670(01)00851-0
Porra R J.2002.The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b.Photosynthesis Research,73(1-3):149-156
Radchenko I G,Il’iash L V.2006.Growth and photosynthetic activity of diatom Thalassiosira weissflogii at decreasing salinity.Izvestiia Akademii Nauk.Seriia Biologicheskaia,(3):306-313
Raven J A.1998.The twelfth tansley lecture,small is beautiful:the picophytoplankton.Functional Ecology,12(4):503-513,doi:10.1046/j.1365-2435.1998.00233.x
Rijstenbil J W,Mur L R,Wijnholds J J,et al.1989a.Impact of a temporal salinity decrease on growth and nitrogen metabolism of the marine diatom Skeletonema costatum in continuous cultures.Marine Biology,101(1):121-129,doi:10.1007/BF00393485
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