Cite this paper:
Caixia WANG, Min WANG, Binbin CHEN, Wenli QIN, Lidong LIN, Chuanjun DAI, Hengguo YU, Renhui LI, Min ZHAO, Zengling MA. Harmful algal bloom-forming dinoflagellate Prorocentrum donghaiense inhibits the growth and photosynthesis of seaweed Sargassum fusiformis embryos[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2237-2251

Harmful algal bloom-forming dinoflagellate Prorocentrum donghaiense inhibits the growth and photosynthesis of seaweed Sargassum fusiformis embryos

Caixia WANG1,2, Min WANG1,2, Binbin CHEN1,2, Wenli QIN1,2, Lidong LIN1,3, Chuanjun DAI1,2, Hengguo YU1,2, Renhui LI1,2, Min ZHAO1,2, Zengling MA1,2
1 Zhejiang Provincial Key Laboratory for Subtropical Water Environment and Marine Biological Resources Protection, Wenzhou University, Wenzhou 325035, China;
2 National and Local Joint Engineering Research Center of Ecological Treatment Technology for Urban Water Pollution, Wenzhou University, Wenzhou 325035, China;
3 Dongtou Fisheries Science and Technology Research Institute, Wenzhou 325700, China
Abstract:
Harmful algal bloom (HAB) is an ecological disaster to local mariculture. At present, its impact on macrophytes has not been well studied. In this study, we cultivated sexually propagated embryos of Sargassum fusiformis— an edible seaweed—in Prorocentrum donghaiense suspensions at different cell densities (0, 0.50×105, 0.75×105, 1.00×105, and 1.50×105 cells/mL) for 10 days, during which growth and photosynthetic activities of the embryos were determined, and a monocultivation was set up for comparison. Results show that the relative growth rate and photosynthetic activities of the embryos co-cultivated with P. donghaiense were inhibited mostly and significantly in the cell densities of 0.75×105, 1.00×105, and 1.50×105 cells/mL, and the inhibitory effects increased in overall with increased cell densities. The maximum relative electron transport rates (rETRmax) and apparent photosynthetic efficiency (α) of co-cultivated embryos were all significantly lower than monocultivation ones on the 10th day. Furthermore, the photosynthetic activity detected by chlorophyll-a fluorescence transient (i.e., OJIP), the electron transport among electron transfer accepters of PSⅡ (photosystem Ⅱ) and that from PSⅡ to PSI (photosystem I) was restricted, which is probably responsible for the decreases of rETRmax and α in the co-cultivated embryos. In addition, parts of the photosynthetic reaction centers of PSⅡ in the co-cultivated embryos were inactivated. Therefore, P. donghaiense bloom could restrain the development and photosynthetic activities of S. fusiformis embryos, reduce the seedlings stock, and eventually hinder the development of S. fusiformis production industry.
Key words:    embryo|JIP-test|photosynthesis|Prorocentrum donghaiense|Sargassum fusiformis|harmful algal bloom   
Received: 2020-10-31   Revised: 2020-12-21
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Articles by Caixia WANG
Articles by Min WANG
Articles by Binbin CHEN
Articles by Wenli QIN
Articles by Lidong LIN
Articles by Chuanjun DAI
Articles by Hengguo YU
Articles by Renhui LI
Articles by Min ZHAO
Articles by Zengling MA
References:
Anderson D M, Cembella A D, Hallegrae G M. 2012. Progress in understanding harmful algal blooms:paradigm shifts and new technologies for research, monitoring, and management. Annual Review of Marine Science, 4:143-176, https://doi.org/10.1146/annurev-marine-120308-081121.
Anderson D M, Glibert P M, Burkholder G J M. 2002. Harmful algal blooms and eutrophication:nutrient sources, composition, and consequences. Estuaries, 25(4):704-726, https://doi.org/10.1007/BF02804901.
Appenroth K J, Stöckel J, Srivastava A, Strasser R J. 2001. Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probed by OJIP chlorophyll a fluorescence measurement. Environmental Pollution, 115(1):49-64, https://doi.org/10.1016/S0269-7491(01)00091-4.
Branch G M, Bustamante R H, Robinson T B. 2013. Impacts of a ‘black tide’ harmful algal bloom on rocky-shore intertidal communities on the West Coast of South Africa. Harmful Algae, 24:54-64, https://doi.org/10.1016/j.hal.2013.01.005.
Chai Z Y, Wang H, Deng Y Y, Hu Z X, Tang Y Z. 2020. Harmful algal blooms significantly reduce the resource use efficiency in a coastal plankton community. Science of the Total Environment, 704:135381, https://doi.org/10.1016/j.scitotenv.2019.135381.
Eilers P H C, Peeters J C H. 1988. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecological Modelling, 42(3-4):199-215, https://doi.org/10.1016/0304-3800(88)90057-9.
Glenn E P, Doty M S. 1992. Water motion affects the growth rates of Kappaphycus alvarezii and related red seaweeds. Aquaculture, 108(3-4):233-246, https://doi.org/10.1016/0044-8486(92)90109-X.
Glibert P M, Burkholder J M, Kana T M. 2012. Recent insights about relationships between nutrient availability, forms, and stoichiometry, and the distribution, ecophysiology, and food web effects of pelagic and benthic Prorocentrum species. Harmful Algae, 14:231-259, https://doi.org/10.1016/j.hal.2011.10.023.
Glibert P M, Icarus Allen J, Artioli Y, Beusen A, Bouwman L, Harle J, Holmes R, Holt J. 2014. Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change:projections based on model analysis. Global Change Biology, 20(12):3845-3858, https://doi.org/10.1111/gcb.12662.
Guillard R R L. 1975. Culture of phytoplankton for feeding marine invertebrates. In:Smith W L, Chanley M H eds. Culture of Marine Invertebrate Animals. Springer, Boston, MA. p.29-60, https://doi.org/10.1007/978-1-4615-8714-9_3.
He X, Bai Y, Pan D, Chen C T A, Cheng Q, Wang D, Gong F. 2013. Satellite views of the seasonal and interannual variability of phytoplankton blooms in the eastern China seas over the past 14 yr (1998-2011). Biogeosciences, 10(7):4721-4739, https://doi.org/10.5194/bg-10-4721-2013.
Hermans C, Smeyers M, Rodriguez R M, Eyletters M, Strasser R J, Delhaye J P. 2003. Quality assessment of urban trees:A comparative study of physiological characterisation, airborne imaging and on site fluorescence monitoring by the OJIP-test. Journal of Plant Physiology, 160(1):81-90, https://doi.org/10.1078/0176-1617-00917.
Howes E L, Joos F, Eakin C M, Gattuso J P. 2015. An updated synthesis of the observed and projected impacts of climate change on the chemical, physical and biological processes in the oceans. Frontiers in Marine Science, 2:36, https://doi.org/10.3389/fmars.2015.00036.
Inaba N, Trainer V L, Onishi Y, Ishii K I, Wyllie-Echeverria S, Imai I. 2017. Algicidal and growth-inhibiting bacteria associated with seagrass and macroalgae beds in Puget Sound, WA, USA. Harmful Algae, 62:136-147, https://doi.org/10.1016/j.hal.2016.04.004.
Kalaji M H, Carpentier R, Allakhverdiev S I, Bosa K. 2012. Fluorescence parameters as early indicators of light stress in barley. Journal of Photochemistry and Photobiology B:Biology, 112:1-6, https://doi.org/10.1016/j.jphotobiol. 2012.03.009.
Kim Y K, Kim S H, Lee K S. 2015. Seasonal growth responses of the seagrass Zostera marina under severely diminished light conditions. Estuaries and Coasts, 38(2):558-568, https://doi.org/10.1007/s12237-014-9833-2.
Kitajima M, Butler W L. 1975. Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochimica et Biophysica Acta(BBA) - Bioenergetics, 376(1):105-115, https://doi.org/10.1016/0005-2728(75)90209-1.
Krumhansl K A, Scheibling R E. 2012. Production and fate of kelp detritus. Marine Ecology Progress Series, 467:281-302, https://doi.org/10.3354/meps09940.
Lin J N, Song J J, Yan T, Zhang Q C, Zhou M J. 2015. Largescale dinoflagellate bloom species Prorocentrum donghaiense and Karenia mikimotoi reduce the survival and reproduction of copepod Calanus sinicus. Journal of the Marine Biological Association of the United Kingdom, 95(6):1071-1079, https://doi.org/10.1017/S0025315415000533.
Lin J N, Yan T, Zhang Q C, Wang Y F, Liu Q, Zhou M J. 2014. In situ detrimental impacts of Prorocentrum donghaiense blooms on zooplankton in the East China Sea. Marine Pollution Bulletin, 88(1-2):302-310, https://doi.org/10.1016/j.marpolbul.2014.08.026.
Lin L D, Shang T G, Zhang T T, Wang C X, Chen B B, Wu M J, Ma Z L. 2020. Supplementary study on reproductive biology and life cycle of Sargassum fusiforme(Phaeophyceae). Journal of Fisheries of China, 44(4):581-595. (in Chinese with English abstract)
Liu S Y, Yu Z M, Song X X, Cao X H. 2017. Effects of modified clay on the physiological and photosynthetic activities of Amphidinium carterae Hulburt. Harmful Algae, 70:64-72, https://doi.org/10.1016/j.hal.2017.10.007.
Lotze H K, Lenihan H S, Bourque B J, Bradbury R H, Cooke R G, Kay M C, Kidwell S M, Kirby M X, Peterson C H, Jackson J B C. 2006. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science, 312(5781):1806-1809, https://doi.org/10.1126/science.1128035.
Lu D D, Goebel J, Qi Y, Zou J Z, Han X T, Gao Y H, Li Y G. 2005. Morphological and genetic study of Prorocentrum donghaiense Lu from the East China Sea, and comparison with some related Prorocentrum species. Harmful Algae, 4(3):493-505, https://doi.org/10.1016/j.hal.2004.08.015.
Lundholm N, Hansen P J, Kotaki Y. 2005. Lack of allelopathIC effects of the domoic acid-producing marine diatom Pseudo-nitzschia multiseries. Marine Ecology Progress Series, 288:21-33, https://doi.org/10.3354/meps288021.
Ma Z L, Lin L D, Wu M J, Yu H G, Shang T G, Zhang T T, Zhao M. 2018. Total and inorganic arsenic contents in seaweeds:Absorption, accumulation, transformation and toxicity. Aquaculture, 497:49-55, https://doi.org/10.1016/j.aquaculture.2018.07.040.
Ma Z L, Shang T G, Zhang T T, Chen B B, Dai X F, Zhao M. 2020. Effects of bloom-forming species dinoflagellate Karenia mikimotoi on the development and photosynthetic characteristics of the sexually propagated embryos of macroalga Sargassum fusiformis. Journal of Applied Phycology, 32(2):1263-1273, https://doi.org/10.1007/s10811-019-02011-4.
Ma Z L, Wu M J, Lin L D, Thring R W, Yu H G, Zhang X, Zhao M. 2017. Allelopathic interactions between the macroalga Hizikia fusiformis (Harvey) and the harmful bloomsforming dinoflagellate Karenia mikimotoi. Harmful Algae, 65:19-26, https://doi.org/10.1016/j.hal.2017.04.003.
Marshall H G. 1995. Succession of dinoflagellate blooms in the Chesapeake Bay, U.S.A. In:Lassus P ed. Harmful Marine Algal Blooms. Intercept Ltd, Andoer. p.615-620.
Moore S K, Johnstone J A, Banas N S, Salathé Jr E P. 2015. Present-day and future climate pathways affecting Alexandrium blooms in Puget Sound, WA, USA. Harmful Algae, 48:1-11, https://doi.org/10.1016/j.hal.2015.06.008.
Pang S J, Gao S Q, Sun J Z. 2006. Cultivation of the brown alga Hizikia fusiformis (Harvey) Okamura:controlled fertilization and early development of seedlings in raceway tanks in ambient light and temperature. Journal of Applied Phycology, 18(6):723-731, https://doi.org/10.1007/s10811-006-9078-y.
Poulin R X, Hogan S, Poulson-Ellestad K L, Brown E, Fernández F M, Kubanek J. 2018. Karenia brevis allelopathy compromises the lipidome, membrane integrity, and photosynthesis of competitors. Scientific Reports, 8(1):9572, https://doi.org/10.1038/s41598-018-27845-9.
Qiu X C, Yamasaki Y, Shimasaki Y, Gunjikake H, Honda M, Kawaguchi M, Matsubara T, Nagasoe S, Etoh T, Matsui S, Honjo T, Oshima Y. 2012. Allelopathy of the raphidophyte Heterosigma akashiwo against the dinoflagellate Akashiwo sanguinea is mediated via allelochemicals and cell contact. Marine Ecology Progress Series, 446:107-118, https://doi.org/10.3354/meps09476.
Sala E, Knowlton N. 2006. Global marine biodiversity trends. Annual Review of Environment and Resources, 31:93-122, https://doi.org/10.1146/annurev.energy.31.020105.100235.
Samborska I A, Kalaji H M, Sieczko L, Goltsev V, Borucki W, Jajoo A. 2018. Structural and functional disorder in the photosynthetic apparatus of radish plants under magnesium deficiency. Functional Plant Biology, 45(6):668-679, https://doi.org/10.1071/FP17241.
Schansker G, Tóth S Z, Kovács L, Holzwarth A R, Garab G. 2011. Evidence for a fluorescence yield change driven by a light-induced conformational change within photosystem Ⅱ during the fast chlorophyll a fluorescence rise. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1807(9):1032-1043, https://doi.org/10.1016/j.bbabio. 2011.05.022.
Schmidt L E, Hansen P J. 2001. Allelopathy in the prymnesiophyte Chrysochromulina polylepis:effect of cell concentration, growth phase and pH. Marine Ecology Progress Series, 216:67-81, https://doi.org/10.3354/meps216067.
Schreiber U. 1998. Chlorophyll Fluorescence:new instruments for special applications. In:Garab G ed. Photosynthesis:Mechanisms and Effects. Kluwer Academic Publishers, Dordrecht. p.4253-4258, https://doi.org/10.1007/978-94-011-3953-3_984.
Shang T G, Lin L D, Chen B B, Wang M, Qin W L, Dai C J, Yu H G, Li J, Thring R W, Ma Z L, Zhao M. 2020. Cell density-dependent suppression on the development and photosynthetic activities of Sargassum fusiformis embryos by dinoflagellate Karenia mikimotoi. Harmful Algae, 96:101842, https://doi.org/10.1016/j.hal.2020.101842.
Shen A, Ishizaka J, Yang M M, Ouyang L L, Yin Y E, Ma Z L. 2019. Changes in community structure and photosynthetic activities of total phytoplankton species during the growth, maintenance, and dissipation phases of a Prorocentrum donghaiense bloom. Harmful Algae, 82:35-43, https://doi.org/10.1016/j.hal.2018.12.007.
Shen A, Xing X L, Li D J. 2015. Allelopathic effects of Prorocentrum donghaiense and Karenia mikimotoi on each other under different temperature. Thalassas, 31(1):33-49.
Smayda T J. 1997. Harmful algal blooms:their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnology and Oceanography, 42(5):1137-1153, https://doi.org/10.4319/lo.1997.42.5_part_2.1137.
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:Mechanisms, Regulation and Adaptation. Taylor and Francis, London. p.445-483.
Strasser R J, Tsimilli-Michael M, Srivastava A. 2004. Analysis of the chlorophyll a fluorescence transient. In:Papageorgiou G C, Govindjee eds. Chlorophyll a fluorescence:A Signature of Photosynthesis. Springer, Dordrecht. p.321-362, https://doi.org/10.1007/978-1-4020-3218-9_12.
Tang D L, Di B P, Wei G F, Ni I H, Oh I S, Wang S F. 2006. Spatial, seasonal and species variations of harmful algal blooms in the South Yellow Sea and East China Sea. Hydrobiologia, 568(1):245-253, https://doi.org/10.1007/s10750-006-0108-1.
Tang Y Z, Gobler C J. 2011. The green macroalga, Ulva lactuca, inhibits the growth of seven common harmful algal bloom species via allelopathy. Harmful Algae, 10(5):480-488, https://doi.org/10.1016/j.hal.2011.03.003.
Thach L B, Shapcott A, Schmidt S, Critchley C. 2007. The OJIP fast fluorescence rise characterizes Graptophyllum species and their stress responses. Photosynthesis Research, 94(2-3):423-436, https://doi.org/10.1007/s11120-007-9207-8.
Tseng C K. 2001. Algal biotechnology industries and research activities in China. Journal of Applied Phycology, 13(4):375-380, https://doi.org/10.1023/A:1017972812576.
Uchida T, Toda S, Matsuyama Y, Yamaguchi M, Kotani Y, Honjo T. 1999. Interactions between the red tide dinoflagellates Heterocapsa circularisquama and Gymnodinium mikimotoi in laboratory culture. Journal of Experimental Marine Biology and Ecology, 241(2):285-299, https://doi.org/10.1016/S0022-0981(99)00088-X.
Van Dolah F M. 2000. Marine algal toxins:origins, health effects, and their increased occurrence. Environmental Health Perspectives, 108(S1):133-141, https://doi.org/10.1289/ehp.00108s1133.
Vredenberg W. 2015. A simple routine for quantitative analysis of light and dark kinetics of photochemical and nonphotochemical quenching of chlorophyll fluorescence in intact leaves. Photosynthesis Research, 124(1):87-106, https://doi.org/10.1007/s11120-015-0097-x.
Wang J H, Wu J Y. 2009. Occurrence and potential risks of harmful algal blooms in the East China Sea. Science of the Total Environment, 407(13):4012-4021, https://doi.org/10.1016/j.scitotenv.2009.02.040.
Wang Y, Tang X X. 2008. Interactions between Prorocentrum donghaiense Lu and Scrippsiella trochoidea (Stein) Loeblich Ⅲ under laboratory culture. Harmful Algae, 7(1):65-75, https://doi.org/10.1016/j.hal.2007.05.005.
Wells M L, Trainer V L, Smayda T J, Karlson B S O, Trick C G, Kudela R M, Ishikawa A, Bernard S, WulffA, Anderson D M, Cochlan W P. 2015. Harmful algal blooms and climate change:learning from the past and present to forecast the future. Harmful Algae, 49:68-93, https://doi.org/10.1016/j.hal.2015.07.009.
Yamasaki Y, Nagasoe S, Matsubara T, Shikata T, Shimasaki Y, Oshima Y, Honjo T. 2007. Growth inhibition and formation of morphologically abnormal cells of Akashiwo sanguinea (Hirasaka) G. Hansen et Moestrup by cell contact with Cochlodinium polykrikoides Margalef. Marine Biology, 152(1):157-163, https://doi.org/10.1007/s00227-007-0671-7.
Yang Y F, Chai Z Y, Wang Q, Chen W Z, He Z L, Jiang S J. 2015. Cultivation of seaweed Gracilaria in Chinese coastal waters and its contribution to environmental improvements. Algal Research, 9:236-244, https://doi.org/10.1016/j.algal.2015.03.017.
Zhao Y F, Yu Z M, Song X X, Cao X H. 2009. Biochemical compositions of two dominant bloom-forming species isolated from the Yangtze River Estuary in response to different nutrient conditions. Journal of Experimental Marine Biology and Ecology, 368(1):30-36, https://doi.org/10.1016/j.jembe.2008.09.023.
Zingone A, Enevoldsen H O. 2000. The diversity of harmful algal blooms:a challenge for science and management. Ocean & Coastal Management, 43(8-9):725-748, https://doi.org/10.1016/S0964-5691(00)00056-9.
Zivcak M, Brestic M, Kalaji M H, Govindjee. 2014. Photosynthetic responses of sun- and shade- grown barley leaves to high light:is the lower PSⅡ connectivity in shade leaves associated with protection against excess of light? Photosynthesis Research, 119(3):339-354, https://doi.org/10.1007/s11120-014-9969-8.
Zivcak M, Brestic M, Kunderlikova K, Olsovska K, Allakhverdiev S I. 2015. Effect of photosystem I inactivation on chlorophyll a fluorescence induction in wheat leaves:does activity of photosystem I play any role in OJIP rise? Journal of Photochemistry and Photobiology B:Biology, 152:318-324, https://doi.org/10.1016/j.jphotobiol.2015.08.024.
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