Cite this paper:
Ni WU, Suping FU, Xinru SONG, Mengmeng TONG, Tianjiu JIANG. Stress regulation of photosynthetic system of Phaeocystis globosa and their hemolytic activity[J]. Journal of Oceanology and Limnology, 2022, 40(6): 2164-2177

Stress regulation of photosynthetic system of Phaeocystis globosa and their hemolytic activity

Ni WU1,2, Suping FU1, Xinru SONG3, Mengmeng TONG3, Tianjiu JIANG1
1 Key Laboratory of Aquatic Eutrophication and Control of Harmful Algal Blooms of Guangdong Higher Education Institute, Research Center of Hydrobiology, Jinan University, Guangzhou 510632, China;
2 South China Sea Institute of Planning and Environmental Research, State Oceanic Administration, Guangzhou 510300, China;
3 Ocean College, Zhejiang University, Zhoushan 316021, China
Abstract:
Blooms of Phaeocystis globosa have been reported accountable for massive fish mortality worldwide. The toxigenic mechanisms of P. globosa, however, remain largely unclear due to the multiple structures and/or synergistic or antagonistic effects of hemolytic compounds. External stressors could lead to the regulation of photoprotective or antioxidative defense system, as well as the potential hemolytic activity. Therefore, the light-induced photosynthetic system, including the accessory photosynthetic growth, the relative electron transfer rate (ETR), photosynthetic efficiency (Fv/Fm), quantum yield of photosystem II (Yield), together with the hemolytic activity of P. globosa were investigated under variable environmental conditions in the present study. Results confirmed that hemolytic activity of P. globosa was initiated by the light, but inhibited by low temperature (16 ℃), high light intensity (>100 μmol/(m2·s)), and iron-limited conditions. Interestingly, the hemolytic activity was not impacted by photosynthetic electron inhibitors (Diuron, atrazine, paraquat, and dibromothymoquinone), which significantly inhibited the photosynthetic activity of P. globosa. The correlated response of hemolytic and photosynthetic activity of P. globosa under those environmental factors suggested that the hemolytic compounds of P. globosa would be involved in the photosynthetic process but not in the electron transfer chain of P. globosa.
Key words:    Phaeocystis globosa|hemolytic activity|photosynthetic system   
Received: 2021-11-16   Revised:
Tools
PDF (802 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Ni WU
Articles by Suping FU
Articles by Xinru SONG
Articles by Mengmeng TONG
Articles by Tianjiu JIANG
References:
Belatik A, Joly D, Hotchandani S et al. 2013. Re-evaluation of the side effects of cytochrome b6f inhibitor dibromothymoquinone on photosystem II excitation and electron transfer. Photosynthesis Research, 117(1-3): 489-496, https://doi.org/10.1007/s11120-013-9798-1.
Bertin M J, Zimba P V, Beauchesne K R et al. 2012. The contribution of fatty acid amides to Prymnesium parvum Carter toxicity. Harmful Algae, 20: 117-125, https://doi.org/10.1016/j.hal.2012.08.004.
Blauw A N, Los F J, Huisman J et al. 2010. Nuisance foam events and Phaeocystis globosa blooms in Dutch coastal waters analyzed with fuzzy logic. Journal of Marine Systems, 83(3-4): 115-126, https://doi.org/10.1016/j.jmarsys.2010.05.003.
Bollivar D W. 2006. Recent advances in chlorophyll biosynthesis. Photosynthesis Research, 89(3): 1-22, https://doi.org/10.1007/s11120-006-9076-6.
Brain R A, Arnie J R, Porch J R et al. 2012. Recovery of photosynthesis and growth rate in green, blue-green, and diatom algae after exposure to atrazine. Environmental Toxicology and Chemistry, 31(11): 2572-2581, https://doi.org/10.1002/etc.1988.
Buchan A, LeCleir G R, Gulvik C A et al. 2014. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nature reviews Microbiology, 12(10): 686-698, https://doi.org/10.1038/nrmicro3326.
Buffan-Dubau E, Carman K R. 2000. Extraction of benthic microalgal pigments for HPLC analyses. Marine Ecology Progress Series, 204: 293-297, https://doi.org/10.3354/meps204293.
Cao J R, Huan Q L, Wu N et al. 2015. Effects of temperature, light intensity and nutrient condition on the growth and hemolytic activity of six species of typical ichthyotoxic algae. Marine Environmental Science, 34(3): 321-329, https://doi.org/10.13634/j.cnki.mes.2015.03.001. (in Chinese with English abstract)
Chen J F, Xu N, Jiang T J, et al. 1999. A report of Phaeocystis globosa bloom in coastal water of Southeast China.Journal-Jinan University Natural Science and Medicine Edition, 20(3):124-129. (in Chinese with English abstract)
de Q Mendes M C, Nunes J M C, Menezes M et al. 2017. Toxin production, growth kinetics and molecular characterization of Ostreopsis cf. ovata isolated from Todos os Santos Bay, tropical southwestern Atlantic. Toxicon, 138: 18-30, https://doi.org/10.1016/j.toxicon.2017.08.007.
Doan H N, Nguyen N L, Nguyen C et al. 2003. Plankton assemblages during the late bloom of Haptophyte algae in Binh Thuan province, Southern central Vietnam, in July 2002. Collection of Marine Research Works, 13: 105-118.
Eschbach E, Scharsack J P, John U et al. 2001. Improved erythrocyte lysis assay in microtitre plates for sensitive detection and efficient measurement of haemolytic compounds from ichthyotoxic algae. Journal of Applied Toxicology, 21(6): 513-519, https://doi.org/10.1002/jat.797.
Gong B, Wu H P, Ma J X et al. 2018. The algae community in taxon Haptophyceae at the early bloom stage of Phaeocystis globosa in Northern Beibu Gulf in winter.BioRxiv, https://doi.org/10.1101/492454.
Guillard R R L. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Smith M L, Chanley M H eds.Culture of Marine Invertebrate Animals. Plenum Press, New York. p.29-60, https://doi.org/10.1007/978-1-4615-8714-9_3.
Guo J, Yang W D, Liu J S et al. 2007. Effects of salinity, temperature and light intensity on the growth and toxin production of Phaeocystis globosa. Acta Scientiae Circumstantiae, 27(8): 1341-1346, https://doi.org/10.3321/j.issn:0253-2468.2007.08.020. (in Chinese with English abstract)
Hai D N, Lam N N, Dippner J W. 2010. Development of Phaeocystis globosa blooms in the upwelling waters of the south central coast of Viet Nam. Journal of Marine Systems, 83(3-4): 253-261, https://doi.org/10.1016/j.jmarsys.2010.04.015.
Hansen E, Ernstsen A, Eilertsen H C. 2004. Isolation and characterisation of a cytotoxic polyunsaturated aldehyde from the marine phytoplankter Phaeocystis pouchetii(Hariot) Lagerheim. Toxicology, 199(2-3): 207-217, https://doi.org/10.1016/j.tox.2004.02.026.
Harrison P J, Waters R E, Taylor F J R. 1980. A broad spectrum artificial sea water medium for coastal and open ocean phytoplankton. Journal of Phycology, 16(1): 28-35, https://doi.org/10.1111/j.0022-3646.1980.00028.x.
He J W, Shi Z X, Zhang Y H et al. 1999. Morphological characteristics and toxins of Phaeocystis CF. Pouchetii(Prymnesiophyceae). Oceanologia et Limnologia Sinica, 30(2): 172-179. (in Chinese with English abstract)
Henrikson J C, Gharfeh M S, Easton A C et al. 2010.Reassessing the ichthyotoxin profile of cultured Prymnesium parvum (golden algae) and comparing it to samples collected from recent freshwater bloom and fish kill events in North America. Toxicon, 55(7): 1396-1404, https://doi.org/10.1016/j.toxicon.2010.02.017.
Hiraga Y, Shikano T, Widianti T et al. 2008. Three new glycolipids with cytolytic activity from cultured marine dinoflagellate Heterocapsa circularisquama.Natural Product Research, 22(8): 649-657, https://doi.org/10.1080/14786410701369417.
Hoogstraten A, Peters M, Timmermans K R et al. 2012.Combined effects of inorganic carbon and light on Phaeocystis globosa Scherffel (Prymnesiophyceae).Biogeosciences, 9(5): 1885-1896, https://doi.org/10.5194/bg-9-1885-2012.
Jiang T, Teng D Q, Jiang T J et al. 2012. Advances in hemolytic toxins of marine microalgae. Journal of Tropical and Subtropical Botany, 20(3): 311-318, https://doi.org/10.3969/j.issn.1005-3395.2012.03.016. (in Chinese with English abstract)
Kang Z J, Yang B, Lai J X et al. 2020. Phaeocystis globosa bloom monitoring: based on P. globosa induced seawater viscosity modification adjacent to a nuclear power plant in Qinzhou Bay, China. Journal of Ocean University of China, 19(5): 1207-1220, https://doi.org/10.1007/s11802-020-4481-6.
Karlson B, Andersen P, Arneborg L et al. 2021. Harmful algal blooms and their effects in coastal seas of Northern Europe. Harmful Algae, 102: 101989, https://doi.org/10.1016/j.hal.2021.101989.
Larson C A, Mirza B, Rodrigues J L M et al. 2018. Iron limitation effects on nitrogen-fixing organisms with possible implications for cyanobacterial blooms. FEMS Microbiology Ecology, 94(5): fiy046, https://doi.org/10.1093/femsec/fiy046.
Lill R. 2009. Function and biogenesis of iron-sulphur proteins.Nature, 460(7257): 831-838, https://doi.org/10.1038/nature08301.
Ling C, Trick C G. 2010. Expression and standardized measurement of hemolytic activity in Heterosigma akashiwo. Harmful Algae, 9(5): 522-529, https://doi.org/10.1016/j.hal.2010.04.004.
Liu D, Zhou M. 2018. Green tides of the Yellow Sea: massive free-floating blooms of Ulva prolifera. In: Glibert P, Berdalet E, Burford M et al eds. Global Ecology and Oceanography of Harmful Algal Blooms. Springer, Cham. p.317-326, https://doi.org/10.1007/978-3-319-70069-4_16.
Liu H X, Huang H H, Xu S N et al. 2015. Planktonic community structure during a harmful bloom of Phaeocystis globosa in a subtropical bay, with special reference to the ciliate assemblages. Ecotoxicology, 24(7-8): 1419-1429, https://doi.org/10.1007/s10646-015-1464-2.
Liu J S, Peng X C, Yang W D. 2006. Growth and hemolytic activities of Phaeocystis globosa Scherffel at different mutrients condition. Acta Ecologica Sinica, 26(3): 780-785, https://doi.org/10.3321/j.issn:1000-0933.2006.03.020. (in Chinese with English abstract)
Liu J S, van Rijssel M, Yang W D et al. 2010. Negative effects of Phaeocystis globosa on microalgae. Chinese Journal of Oceanology and Limnology, 28(4): 911-916, https://doi.org/10.1007/s00343-010-9061-y.
Liu S X, Yu Z G, Yao P et al. 2011. Effects of irradiance on pigment signatures of harmful algae during growth process. Acta Oceanologica Sinica, 30(6): 46-57, https://doi.org/10.1007/s13131-011-0160-1.
Maat D S, de Blok R, Brussaard C P D. 2016. Combined phosphorus limitation and light stress prevent viral proliferation in the phytoplankton species Phaeocystis globosa, but not in Micromonas pusilla. Frontiers in Marine Science, 3: 160, https://doi.org/10.3389/fmars.2016.00160.
Madhupratap M, Sawant S, Gauns M. 2000. A first report on a bloom of the marine prymnesiophycean, Phaeocystis globosa from the Arabian Sea. Oceanologica Acta, 23(1):83-90, https://doi.org/10.1016/S0399-1784(00)00109-2.
Mao H B, Li G F, Ruan X et al. 2002. The redox state of plastoquinone pool regulates state transitions via cytochrome b6f complex in Synechocystis sp. PCC 6803.FEBS Letters, 519(1-3): 82-86, https://doi.org/10.1016/S0014-5793(02)02715-1.
Masotti I, Belviso S, Alvain S et al. 2010. Spatial and temporal variability of the dimethylsulfide to chlorophyll ratio in the surface ocean: an assessment based on phytoplankton group dominance determined from space. Biogeosciences, 7(10): 3215-3237, https://doi.org/10.5194/bg-7-3215-2010.
Mohapatra B R, Rellinger A N, Kieber D J et al. 2013.Comparative functional characteristics of DMSP lyases extracted from polar and temperate Phaeocystis species.Aquatic Biology, 18(2): 185-195, https://doi.org/10.3354/ab00504.
Mohapatra B R, Rellinger A N, Kieber D J et al. 2014.Kinetics of DMSP lyases in whole cell extracts of four Phaeocystis species: response to temperature and DMSP analogs. Journal of Sea Research, 86: 110-115, https://doi.org/10.1016/j.seares.2013.11.012.
Moisan T A, Ellisman M H, Buitenhuys C W et al. 2006.Differences in chloroplast ultrastructure of Phaeocystis antarctica in low and high light. Marine Biology, 149(6):1281-1290, https://doi.org/10.1007/s00227-006-0321-5.
Nejstgaard J C, Tang K W, Steinke M et al. 2007. Zooplankton grazing on Phaeocystis: a quantitative review and future challenges. Biogeochemistry, 83(1-3): 147-172, https://doi.org/10.1007/s10533-007-9098-y.
Peperzak L, Gäbler-Schwarz S. 2012. Current knowledge of the life cycles of Phaeocystis globosa and Phaeocystis antarctica (Prymnesiophyceae). Journal of Phycology, 48(3): 514-517, https://doi.org/10.1111/j.1529-8817.2012. 01136.x.
Peperzak L, Poelman M. 2008. Mass mussel mortality in The Netherlands after a bloom of Phaeocystis globosa(Prymnesiophyceae). Journal of Sea Research, 60(3):220-222, https://doi.org/10.1016/j.seares.2008.06.001.
Pohnert G. 2005. Diatom/copepod interactions in plankton:the indirect chemical defense of unicellular algae.ChemBioChem, 6(6): 946-959, https://doi.org/10.1002/cbic.200400348.
Qi Y Z, Chen J F, Wang Z H et al. 2004. Some observations on harmful algal bloom (HAB) events along the coast of Guangdong, Southern China in 1998.Hydrobiologia, 512(1): 209-214, https://doi.org/10.1023/B:HYDR.0000020329.06666.8c.
Roberts A G, Bowman M K, Kramer D M. 2004. The inhibitor DBMIB provides insight into the functional architecture of the Q0 site in the cytochrome b6f complex. Biochemistry, 43(24): 7707-7716, https://doi.org/10.1021/bi049521f.
Schoemann V, Becquevort S, Stefels J et al. 2005. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. Journal of Sea Research, 53(1-2):43-66, https://doi.org/10.1016/j.seares.2004.01.008.
Selleslagh J, Amara R. 2008. Inter-season and interannual variations in fish and macrocrustacean community structure on a eastern English Channel Sandy beach:influence of environmental factors. Estuarine, Coastal and Shelf Science, 77(4): 721-730, https://doi.org/10.1016/j.ecss.2007.11.004.
Seoane S, Zapata M, Orive E. 2009. Growth rates and pigment patterns of haptophytes isolated from estuarine waters.Journal of Sea Research, 62(4): 286-294, https://doi.org/10.1016/j.seares.2009.07.008.
Sheehan C E, Petrou K. 2020. Dimethylated sulfur production in batch cultures of Southern Ocean phytoplankton.Biogeochemistry, 147(1): 53-69, https://doi.org/10.1007/s10533-019-00628-8.
Sheik A R, Brussaard C P D, Lavik G et al. 2014. Responses of the coastal bacterial community to viral infection of the algae Phaeocystis globosa. ISME Journal, 8(1): 212-225, https://doi.org/10.1038/ismej.2013.135.
Shen P P, Qi Y Z, Ou L J. 2018. Phaeocystis globosa in coastal China: taxonomy, distribution, and its blooms. Marine Sciences, 42(10): 146-162, https://doi.org/10.11759/hykx20171225004. (in Chinese with English abstract)
Shen P P, Qi Y Z, Wang Y et al. 2011. Phaeocystis globosa Scherffel, a harmful microalga, and its production of dimethylsulfoniopropionate. Chinese Journal of Oceanology and Limnology, 29(4): 869-873, https://doi.org/10.1007/s00343-011-0515-7.
Slagter H A, Gerringa L J A, Brussaard C P D. 2016.Phytoplankton virus production negatively affected by iron limitation. Frontiers in Marine Science, 3: 156, https://doi.org/10.3389/fmars.2016.00156.
Trebst A. 2007. Inhibitors in the functional dissection of the photosynthetic electron transport system. Photosynthesis Research, 92(2): 217-224, https://doi.org/10.1007/s11120-007-9213-x.
Twiner M J, Trick C G. 2000. Possible physiological mechanisms for production of hydrogen peroxide by the ichthyotoxic flagellate Heterosigma akashiwo. Journal of Plankton Research, 22(10): 1961-1975, https://doi.org/10.1093/plankt/22.10.1961.
Van Leeuwe M A, Stefels J. 2007. Photosynthetic responses in Phaeocystis antarctica towards varying light and iron conditions. Biogeochemistry, 83(1-3): 61-70, https://doi.org/10.1007/s10533-007-9083-5.
Van Leeuwe M A, Visser R J W, Stefels J. 2014. The pigment composition of Phaeocystis antarctica (Haptophyceae)under various conditions of light, temperature, salinity, and iron. Journal of Phycology, 50(6): 1070-1080, https://doi.org/10.1111/jpy.12238.
Wan L L, Zhou Q X, Wang X et al. 2019. Cu2O nanocubes with mixed oxidation-state facets for (photo) catalytic hydrogenation of carbon dioxide. Nature Catalysis, 2(10):889-898, https://doi.org/10.1038/s41929-019-0338-z.
Wang X D, Song H Y, Wang Y et al. 2021. Research on the biology and ecology of the harmful algal bloom species Phaeocystis globosa in China: progresses in the last 20 years. Harmful Algae, 107: 102057, https://doi.org/10.1016/j.hal.2021.102057.
Wang X D, Wang Y, Ou L J. 2014. The roles of light-dark cycles in the growth of Phaeocystis globosa from the South China Sea: the cost of colony enlargement. Journal of Sea Research, 85: 518-523, https://doi.org/10.1016/j.seares.2013.08.009.
Wang X J, Feng X Q, Zhuang Y et al. 2019. Effects of ocean acidification and solar ultraviolet radiation on physiology and toxicity of dinoflagellate Karenia mikimotoi. Harmful Algae, 81: 1-9, https://doi.org/10.1016/j.hal.2018.11.013.
Xu N, Huang B Z, Hu Z X et al. 2017. Effects of temperature, salinity, and irradiance on the growth of harmful algal bloom species Phaeocystis globosa Scherffel(Prymnesiophyceae) isolated from the South China Sea.Chinese Journal of Oceanology and Limnology, 35(3):557-565, https://doi.org/10.1007/s00343-017-5352-x.
Xu Y X, He X L, Zhang T et al. 2020. Causative species of Phaeocystis blooms in Beibu Gulf. Journal of Tropical Oceanography, 30(6): 122-130, https://doi.org/10.11978/2020030. (in Chinese with English abstract)
Yan G J, Ding Q Y, Gao X C. 2019. The effect of temperature, salinity and light intensity on growth and methyl halides production of Phaeocystis globose. Periodical of ocean university of China, 49(2): 67-73, https://doi.org/10.16441/j.cnki.hdxb.20180057. (in Chinese with English abstract)
Yang Q X, Chen L N, Hu X L et al. 2015. Toxic effect of a marine bacterium on aquatic organisms and its algicidal substances against Phaeocystis globosa. PLoS One, 10(2):e0114933, https://doi.org/10.1371/journal.pone.0114933.
Yang W D, Shang W, Liu J S. 2009. Acute toxicities of Phaeocystis globosa on five aquatic animals. Journal of Tropical and Subtropical Botany, 17(1): 68-73, https://doi.org/10.3969/j.issn.1005-3395.2009.01.012. (in Chinese with English abstract)
Zapata M, Garrido J L. 1991. Influence of injection conditions in reversed-phase high-performance liquid chromatography of chlorophylls and carotenoids. Chromatographia, 31(11-12): 589-594, https://doi.org/10.1007/BF02279480.
Zapata M, Jeffrey S W, Wright S W et al. 2004. Photosynthetic pigments in 37 species (65 strains) of Haptophyta:implications for oceanography and chemotaxonomy.Marine Ecology Progress Series, 270: 83-102, https://doi.org/10.3354/meps270083.
Zapata M, Rodríguez F, Garrido J L. 2000. Separation of chlorophylls and carotenoids from marine phytoplankton:a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Marine Ecology Progress Series, 195: 29-45, https://doi.org/10.3354/meps195029.
Zhang H J, Wang H, Zheng W et al. 2017. Toxic effects of prodigiosin secreted by Hahella sp. KA22 on harmful alga Phaeocystis globosa. Frontiers in Microbiology, 8:999, https://doi.org/10.3389/fmicb.2017.00999.
Zhou Q X, Ma S L, Zhan S H. 2018. Superior photocatalytic disinfection effect of Ag-3D ordered mesoporous CeO2 under visible light. Applied Catalysis B: Environmental, 224: 27-37, https://doi.org/10.1016/j.apcatb.2017.10.032.
Zhu R, Yang G P, Yu Y et al. 2013. Effects of different N/P ratios and concentration of iron on DMS and DMSP production in the culture of Phaeocystis globosa. Periodical of Ocean University of China, 43(10): 67-75, https://doi.org/10.16441/j.cnki.hdxb.2013.10.010. (in Chinese with English abstract)
Zhuang L E, Zhao L, Yin P H. 2018. Combined algicidal effect of urocanic acid, N-acetylhistamine and L-histidine to harmful alga Phaeocystis globosa. RSC Advances, 8(23):12760-12766, https://doi.org/10.1039/c8ra00749g.
Copyright © Haiyang Xuebao