{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,20]],"date-time":"2026-08-20T14:40:48Z","timestamp":1787236848904,"version":"build-2736575974"},"reference-count":88,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2026,5,9]],"date-time":"2026-05-09T00:00:00Z","timestamp":1778284800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["42376211"],"award-info":[{"award-number":["42376211"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"award":["42376211"],"award-info":[{"award-number":["42376211"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"name":"Cyrus Tang fundation","award":["M. Tong"],"award-info":[{"award-number":["M. Tong"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Toxins"],"abstract":"<jats:p>Chattonella marina is an ichthyotoxic, bloom-forming raphidophyte known for its hemolytic activity. However, the mechanisms by which nitrogen (N) and phosphorus (P) limitation influence this hemolytic toxicity remain poorly understood. In this study, both N and P limitation reduced growth, photosynthetic efficiency (Fv\/Fm, YII, rETRmax), and the expression of nutrient-uptake, tetrapyrrole\/chlorophyll biosynthesis genes. Nevertheless, the two nutrients produced opposite effects on toxicity: N limitation lowered hemolytic activity and ROS levels to near zero, whereas P limitation kept both relatively high, similar to nutrient-replete controls. The addition of the antioxidant NAC (N-Acetyl-L-cysteine) reduced hemolytic activity, confirming that ROS contributes to toxicity. Transcriptome data showed that under N limitation, genes for nitrogen uptake and initial reduction (NRT, NR, glnA) were upregulated, while downstream assimilation genes (nirA, GLT1) were downregulated. In contrast, under P limitation, all the nitrogen-metabolism-related genes (NRT, NR, glnA, nirA, GLT1) were downregulated. In the tetrapyrrole pathway, most genes were downregulated under both nutrient-limited conditions, except for HemD, suggesting a bottleneck that may result in the accumulation of porphyrin intermediates within the tetrapyrrole\/chlorophyll biosynthesis pathway. Together, the secondary products derived primarily from the reaction of ROS with tetrapyrrole-based compounds appear to be the main contributors to hemolytic toxicity. Consequently, high levels of both ROS and porphyrin intermediates under P-limited conditions, as well as high ROS levels but low porphyrin intermediates under nutrient-sufficient conditions, may both contribute to the high hemolytic toxicity of C. marina. In contrast, under N limitation, despite the accumulation of porphyrin intermediates, the strong suppression of photosynthetic electron transport limits both ROS production and the synthesis of nitrogen-containing toxins, resulting in low hemolytic activity. These findings demonstrate that nutrient conditions regulate hemolytic activity in C. marina in a nutrient-specific manner.<\/jats:p>","DOI":"10.3390\/toxins18050226","type":"journal-article","created":{"date-parts":[[2026,5,11]],"date-time":"2026-05-11T13:10:42Z","timestamp":1778505042000},"page":"226","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Response of Hemolytic and Photosynthetic Activity of Chattonella marina Complex Under Variable N:P Stoichiometry"],"prefix":"10.3390","volume":"18","author":[{"given":"Xinyi","family":"Wang","sequence":"first","affiliation":[{"name":"Food and Pharmacy Institute, Zhejiang Ocean University, Zhoushan 316022, China"},{"name":"Ocean College, Zhejiang University, Zhoushan 316021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kehan","family":"Yi","sequence":"additional","affiliation":[{"name":"Ocean College, Zhejiang University, Zhoushan 316021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5419-7345","authenticated-orcid":false,"given":"Yongjun","family":"Jiang","sequence":"additional","affiliation":[{"name":"Food and Pharmacy Institute, Zhejiang Ocean University, Zhoushan 316022, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5794-8722","authenticated-orcid":false,"given":"Mengmeng","family":"Tong","sequence":"additional","affiliation":[{"name":"Ocean College, Zhejiang University, Zhoushan 316021, China"},{"name":"Hainan Institute, Zhejiang University, Sanya 572025, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,5,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"281","DOI":"10.4490\/algae.2022.37.11.30","article-title":"Quantification of the ichthyotoxic raphidophyte Chattonella marina complex by applying a droplet digital PCR","volume":"37","author":"Min","year":"2022","journal-title":"Algae"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.hal.2011.10.014","article-title":"Life cycle, physiology, ecology and red tide occurrences of the fish-killing raphidophyte Chattonella","volume":"14","author":"Imai","year":"2012","journal-title":"Harmful Algae"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1016\/j.hal.2004.12.008","article-title":"High toxicity of the novel bloom-forming species Chattonella ovata (Raphidophyceae) to cultured fish","volume":"4","author":"Hiroishi","year":"2005","journal-title":"Harmful Algae"},{"key":"ref_4","first-page":"7","article-title":"Fish mortality associated with Chattonella marina and C. cf. ovata (Raphidophyceae) blooms in Sinaloa (Mexico)","volume":"31","author":"Alonso","year":"2006","journal-title":"Harmful Algae News"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Garc\u00eda-Mendoza, E., C\u00e1ceres-Mart\u00ednez, J., Rivas, D., Fimbres-Martinez, M., S\u00e1nchez-Bravo, Y., V\u00e1squez-Yeomans, R., and Medina-Elizalde, J. (2018). Mass mortality of cultivated northern bluefin tuna Thunnus thynnus orientalis associated with Chattonella species in Baja California, Mexico. Front. Mar. Sci., 5.","DOI":"10.3389\/fmars.2018.00454"},{"key":"ref_6","first-page":"321","article-title":"Interspecies competition between Chattonella marina and three typical marine diatoms","volume":"38","author":"Liao","year":"2019","journal-title":"Mar. Environ. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"101787","DOI":"10.1016\/j.hal.2020.101787","article-title":"Harmful algal blooms and associated fisheries damage in East Asia: Current status and trends in China, Japan, Korea and Russia","volume":"102","author":"Sakamoto","year":"2021","journal-title":"Harmful Algae"},{"key":"ref_8","first-page":"57","article-title":"Monospecific bloom of noxious raphidophyte Chattonella marina in the coastal water of south west coast of India","volume":"1","author":"Padmakumar","year":"2011","journal-title":"Int. J. Biosci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"101848","DOI":"10.1016\/j.hal.2020.101848","article-title":"Overview of Australian and New Zealand harmful algal species occurrences and their societal impacts in the period 1985 to 2018, including a compilation of historic records","volume":"102","author":"Hallegraeff","year":"2021","journal-title":"Harmful Algae"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1809","DOI":"10.1093\/plankt\/21.10.1809","article-title":"Comparative ecophysiology of the harmful alga Chattonella marina (Raphidophyceae) from South Australian and Japanese waters","volume":"21","author":"Marshall","year":"1999","journal-title":"J. Plankton Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1016\/j.hal.2005.09.001","article-title":"Bottom-up controls on a mixed-species HAB assemblage: A comparison of sympatric Chattonella subsalsa and Heterosigma akashiwo (Raphidophyceae) isolates from the Delaware Inland Bays, USA","volume":"5","author":"Zhang","year":"2006","journal-title":"Harmful Algae"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"101975","DOI":"10.1016\/j.hal.2021.101975","article-title":"Marine harmful algal blooms (HABs) in the United States: History, current status and future trends","volume":"102","author":"Anderson","year":"2021","journal-title":"Harmful Algae"},{"key":"ref_13","first-page":"337","article-title":"The causative mechanism of Chattonella marina bloom in Dapeng Bay, the south China Sea","volume":"28","author":"Qi","year":"1997","journal-title":"Oceanol. Limnol. Sin."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/S1568-9883(03)00046-5","article-title":"Ichthyotoxicity of Chattonella marina (Raphidophyceae) to damselfish (Acanthochromis polycanthus): The synergistic role of reactive oxygen species and free fatty acids","volume":"2","author":"Marshall","year":"2003","journal-title":"Harmful Algae"},{"key":"ref_15","first-page":"99","article-title":"Progress in the study of toxicological mechanism of Chattonella marina","volume":"28","author":"Gao","year":"2009","journal-title":"Mar. Sci. Bull."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1007\/BF00356281","article-title":"Neurotoxin-induced cardiac disorder and its role in the death of fish exposed to Chattonella marina","volume":"112","author":"Endo","year":"1992","journal-title":"Mar. Biol."},{"key":"ref_17","first-page":"137","article-title":"Properties of neurotoxins separated from a harmful red tide organism Chattonella marina","volume":"47","author":"Khan","year":"1995","journal-title":"Isr. J. Aquac."},{"key":"ref_18","first-page":"297","article-title":"Isolation and characterization of light-dependent hemolytic cytotoxin from harmful red tide phytoplankton Chattonella marina","volume":"141","author":"Kuroda","year":"2005","journal-title":"Comp. Biochem. Physiol. C"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1267\/ahc.16.232","article-title":"Effects of sea bloom, Chattonella antiqua, on gill primary lamellae of the young yellowtail, Seriola quinqueradiata","volume":"16","author":"Shimada","year":"1983","journal-title":"Acta Histochem. Cytochem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1007\/BF00539428","article-title":"Histological and histochemical changes in the gills of the yellowtail Seriola quinqueradiata exposed to the Raphidophycean flagellate Chattonella marina","volume":"87","author":"Endo","year":"1985","journal-title":"Mar. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1351","DOI":"10.2331\/suisan.52.1351","article-title":"Changes in the gill carbonic anhydrase activity of fish exposed to Chattonella marina red tide, with special reference to the mortality","volume":"52","author":"Sakai","year":"1986","journal-title":"Nippon Suisan Gakkaishi"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1093\/plankt\/16.2.161","article-title":"Generation of superoxide anion radicals by the marine phytoplankton organism, Chattonella antiqua","volume":"16","author":"Tanaka","year":"1994","journal-title":"J. Plankton Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"836","DOI":"10.2331\/fishsci.62.836","article-title":"Oxygen radicals are probably involved in the mortality of yellowtail by Chattonella marina","volume":"62","author":"Ishimatsu","year":"1996","journal-title":"Fish. Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1007\/s00227-005-1597-6","article-title":"Superoxide production by marine microalgae","volume":"147","author":"Marshall","year":"2005","journal-title":"Mar. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1007\/s00227-005-1596-7","article-title":"Superoxide production by marine microalgae: I. Survey of 37 species from 6 classes","volume":"147","author":"Marshall","year":"2005","journal-title":"Mar. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Cho, K., Ueno, M., Liang, Y., Kim, D., and Oda, T. (2022). Generation of Reactive Oxygen Species (ROS) by Harmful Algal Bloom (HAB)-Forming Phytoplankton and Their Potential Impact on Surrounding Living Organisms. Antioxidants, 11.","DOI":"10.3390\/antiox11020206"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Wu, N., Tong, M., Gou, S., Zeng, W., Xu, Z., and Jiang, T. (2021). Hemolytic Activity in Relation to the Photosynthetic System in Chattonella marina and Chattonella ovata. Mar. Drugs, 19.","DOI":"10.3390\/md19060336"},{"key":"ref_28","first-page":"321","article-title":"Effects of temperature, light intensity and nutrient condition on the growth and hemolytic activity of six species of typical ichthyotoxic algae","volume":"34","author":"Cao","year":"2015","journal-title":"Mar. Environ. Sci."},{"key":"ref_29","first-page":"1190","article-title":"Effects of temperature, salinity, and light intensity on the grow and toxin production of Chattonella marina","volume":"20","author":"Huang","year":"2009","journal-title":"Chin. J. Appl. Ecol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1014","DOI":"10.1126\/science.1167755","article-title":"Controlling eutrophication: Nitrogen and phosphorus","volume":"323","author":"Conley","year":"2009","journal-title":"Science"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.dsr.2015.12.006","article-title":"Spatial variability of phosphate and nitrate in the Mediterranean Sea: A modeling approach","volume":"108","author":"Lazzari","year":"2016","journal-title":"Deep Sea Res. I"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1002\/lol2.10314","article-title":"Potential drivers and consequences of regional phosphate depletion in the western subtropical North Pacific","volume":"8","author":"Yuan","year":"2023","journal-title":"Limnol. Oceanogr. Lett."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1002\/lno.12541","article-title":"Switches between nitrogen limitation and nitrogen\u2013phosphorus co-limitation in the subtropical North Atlantic Ocean","volume":"69","author":"Yuan","year":"2024","journal-title":"Limnol. Oceanogr."},{"key":"ref_34","first-page":"18","article-title":"Studies on phytoplankton community change at daya bay during a red tide","volume":"24","author":"Li","year":"2005","journal-title":"J. Trop. Oceanogr."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1146\/annurev.arplant.57.032905.105448","article-title":"Tetrapyrrole Biosynthesis in Higher Plants","volume":"58","author":"Tanaka","year":"2007","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1172","DOI":"10.3390\/life5021172","article-title":"Evolutionary Aspects and Regulation of Tetrapyrrole Biosynthesis in Cyanobacteria under Aerobic and Anaerobic Environments","volume":"5","author":"Fujita","year":"2015","journal-title":"Life"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"e00048-16","DOI":"10.1128\/MMBR.00048-16","article-title":"Prokaryotic Heme Biosynthesis: Multiple Pathways to a Common Essential Product","volume":"81","author":"Dailey","year":"2017","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"20120262","DOI":"10.1098\/rstb.2012.0262","article-title":"Controlling the delicate balance of tetrapyrrole biosynthesis","volume":"368","author":"Yin","year":"2013","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1515\/hsz-2020-0308","article-title":"Thioredoxin-dependent control balances the metabolic activities of tetrapyrrole biosynthesis","volume":"402","author":"Wittmann","year":"2021","journal-title":"Biol. Chem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"4624","DOI":"10.1093\/jxb\/erac203","article-title":"Post-translational regulation of metabolic checkpoints in plant tetrapyrrole biosynthesis","volume":"73","author":"Wang","year":"2022","journal-title":"J. Exp. Bot."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1080\/09670269810001736813","article-title":"Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation","volume":"33","author":"Geider","year":"1998","journal-title":"Eur. J. Phycol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1111\/j.0022-3646.1997.00980.x","article-title":"Autolysis kinetics of the marine diatom Ditylum brightwellii (Bacillariophyceae) under nitrogen and phosphorus limitation and starvation","volume":"33","author":"Brussaard","year":"1997","journal-title":"J. Phycol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1584","DOI":"10.4319\/lo.1997.42.7.1584","article-title":"Growth and reproduction of Daphnia galeata in response to changes in fatty acids, phosphorus, and nitrogen in Chlamydomonas reinhardtii","volume":"42","author":"Weers","year":"1997","journal-title":"Limnol. Oceanogr."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"129","DOI":"10.4319\/lo.1998.43.1.0129","article-title":"Physiological stress and cell death in marine phytoplankton: Induction of proteases in response to nitrogen or light limitation","volume":"43","author":"Berges","year":"1998","journal-title":"Limnol. Oceanogr."},{"key":"ref_45","first-page":"11","article-title":"Growth dynamics and toxicity of Alexandrium fundyense (Dinophyceae): The effect of changing N:P supply ratios on internal toxin and nutrient levels","volume":"35","author":"John","year":"2000","journal-title":"Eur. J. Phycol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1038\/nrmicro956","article-title":"Cell death in planktonic, photosynthetic microorganisms","volume":"2","author":"Bidle","year":"2004","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1104\/pp.88.3.923","article-title":"Effects of Growth Irradiance and Nitrogen Limitation on Photosynthetic Energy Conversion in Photosystem II 1","volume":"88","author":"Kolber","year":"1988","journal-title":"Plant Physiol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Liefer, J.D., Garg, A., Campbell, D.A., Irwin, A.J., and Finkel, Z.V. (2018). Nitrogen starvation induces distinct photosynthetic responses and recovery dynamics in diatoms and prasinophytes. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0195705"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1016\/j.algal.2015.04.023","article-title":"The effect of nitrogen limitation on the physiology and metabolism of Chlorella vulgaris var L3","volume":"10","author":"Ikaran","year":"2015","journal-title":"Algal Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1111\/php.13386","article-title":"Nitrogen Limitation Decreases the Repair Capacity and Enhances Photoinhibition of Photosystem II in a Diatom","volume":"97","author":"Li","year":"2021","journal-title":"Photochem. Photobiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1104\/pp.111.184333","article-title":"The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants","volume":"158","author":"Hockin","year":"2012","journal-title":"Plant Physiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1016\/j.algal.2018.09.023","article-title":"Allelochemicals from Alexandrium minutum induce rapid inhibition of metabolism and modify the membranes from Chaetoceros muelleri","volume":"35","author":"Long","year":"2018","journal-title":"Algal Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"111839","DOI":"10.1016\/j.jphotobiol.2020.111839","article-title":"Extracellular secretion of superoxide is regulated by photosynthetic electron transport in the noxious red-tide-forming raphidophyte Chattonella antiqua","volume":"205","author":"Yuasa","year":"2020","journal-title":"J. Photochem. Photobiol. B"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1007\/s10811-015-0652-z","article-title":"Impact of nitrogen limitation on biomass, photosynthesis, and lipid accumulation in Chlorella sorokiniana","volume":"28","author":"Negi","year":"2016","journal-title":"J. Appl. Phycol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1104\/pp.17.01624","article-title":"The impacts of phosphorus deficiency on the photosynthetic electron transport chain","volume":"177","author":"Carstensen","year":"2018","journal-title":"Plant Physiol."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Lovio-Fragoso, J.P., de Jes\u00fas-Campos, D., L\u00f3pez-El\u00edas, J.A., Medina-Ju\u00e1rez, L.\u00c1., Fimbres-Olivarr\u00eda, D., and Hayano-Kanashiro, C. (2021). Biochemical and Molecular Aspects of Phosphorus Limitation in Diatoms and Their Relationship with Biomolecule Accumulation. Biology, 10.","DOI":"10.3390\/biology10070565"},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Bossa, R., Di Colandrea, M., Salbitani, G., and Carfagna, S. (2024). Phosphorous Utilization in Microalgae: Physiological Aspects and Applied Implications. Plants, 13.","DOI":"10.3390\/plants13152127"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/s11120-021-00828-0","article-title":"Nitrogen, phosphorus and high CO2 modulate photosynthesis, biomass and lipid production in the green alga Chlorella vulgaris","volume":"148","author":"Kumari","year":"2021","journal-title":"Photosynth. Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1048","DOI":"10.1007\/s00343-011-0224-2","article-title":"Photosynthetic efficiency, cell volume, and elemental stoichiometric ratios in Thalassirosira weissflogii under phosphorus limitation","volume":"29","author":"Liu","year":"2011","journal-title":"Chin. J. Oceanol. Limnol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.seares.2013.02.007","article-title":"A comparative study of maximal quantum yield of photosystem II to determine nitrogen and phosphorus limitation on two marine algae","volume":"80","author":"Qi","year":"2013","journal-title":"J. Sea Res."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Cui, Y., Zhang, H., and Lin, S. (2017). Enhancement of non-photochemical quenching as an adaptive strategy under phosphorus deprivation in the dinoflagellate Karlodinium veneficum. Front. Microbiol., 8.","DOI":"10.3389\/fmicb.2017.00404"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1558","DOI":"10.1104\/pp.125.4.1558","article-title":"Non-photochemical quenching.A response to excess light energy","volume":"125","author":"Li","year":"2001","journal-title":"Plant Physiol."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Montuori, E., Lima, S., Marchese, A., Scargiali, F., and Lauritano, C. (2024). Lutein Production and Extraction from Microalgae: Recent Insights and Bioactive Potential. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25052892"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Yang, Y., Li, W., Li, Y., and Xu, N. (2024). Effects of ocean acidification and nitrogen limitation on the growth and photophysiological performances of marine macroalgae Gracilariopsis lemaneiformis. Front. Mar. Sci., 11.","DOI":"10.3389\/fmars.2024.1453569"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/S0304-4165(00)00161-6","article-title":"Mechanism of superoxide anion generation in the toxic red tide phytoplankton Chattonella marina: Possible involvement of NAD(P)H oxidase","volume":"1524","author":"Kim","year":"2000","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"102712","DOI":"10.1016\/j.hal.2024.102712","article-title":"Production of extracellular superoxide contributes to photosynthesis via elimination of reducing power and regeneration of NADP(+) in the red-tide-forming raphidophyte Chattonella marina complex","volume":"139","author":"Yuasa","year":"2024","journal-title":"Harmful Algae"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1093\/plankt\/24.11.1231","article-title":"Photosynthesis does influence superoxide production in the ichthyotoxic alga Chattonella marina (Raphidophyceae)","volume":"24","author":"Marshall","year":"2002","journal-title":"J. Plankton Res."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.freeradbiomed.2016.04.001","article-title":"Mitochondrial generation of superoxide and hydrogen peroxide as the source of mitochondrial redox signaling","volume":"100","author":"Brand","year":"2016","journal-title":"Free Radic. Biol. Med."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/j.toxicon.2003.09.012","article-title":"Chemical characterisation of three haemolytic compounds from the microalgal species Fibrocapsa japonica (Raphidophyceae)","volume":"43","author":"Fu","year":"2004","journal-title":"Toxicon"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1104\/pp.114.250530","article-title":"The regulation of photosynthetic structure and function during nitrogen deprivation in Chlamydomonas reinhardtii","volume":"167","author":"Juergens","year":"2015","journal-title":"Plant Physiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/j.bbabio.2006.02.002","article-title":"Glycerate-3-phosphate, produced by CO2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II","volume":"1757","author":"Takahashi","year":"2006","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1007\/s11120-016-0301-7","article-title":"Interactive effects of nitrogen and light on growth rates and RUBISCO content of small and large centric diatoms","volume":"131","author":"Li","year":"2017","journal-title":"Photosynth. Res."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/S0166-445X(01)00191-6","article-title":"Photosensitizing hemolytic toxin in Heterocapsa circularisquama, a newly identified harmful red tide dinoflagellate","volume":"56","author":"Sato","year":"2002","journal-title":"Aquat. Toxicol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1590\/S0100-879X1999000300002","article-title":"The photodynamic and non-photodynamic actions of porphyrins","volume":"32","author":"Afonso","year":"1999","journal-title":"Braz. J. Med. Biol. Res."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"954","DOI":"10.1039\/c8pp00092a","article-title":"Structure\u2013activity relationship of porphyrin-induced photoinactivation with membrane function in bacteria and erythrocytes","volume":"17","author":"Kato","year":"2018","journal-title":"Photochem. Photobiol. Sci."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.hal.2016.08.003","article-title":"Lethal effects of ichthyotoxic raphidophytes, Chattonella marina, C. antiqua, and Heterosigma akashiwo, on post-embryonic stages of the Japanese pearl oyster, Pinctada fucata martensii","volume":"59","author":"Basti","year":"2016","journal-title":"Harmful Algae"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.hal.2018.05.006","article-title":"Chattonella subsalsa (Raphidophyceae) growth and hemolytic activity in response to agriculturally-derived estuarine contaminants","volume":"76","author":"Flood","year":"2018","journal-title":"Harmful Algae"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"2139","DOI":"10.1007\/s00253-021-11147-8","article-title":"Effect of pluronic block polymers and N-acetylcysteine culture media additives on growth rate and fatty acid composition of six marine microalgae species","volume":"105","author":"Sauvage","year":"2021","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"199","DOI":"10.3354\/ame01570","article-title":"Reactive oxygen species are linked to the toxicity of the dinoflagellate Alexandrium spp. to protists","volume":"66","author":"Flores","year":"2012","journal-title":"Aquat. Microb. Ecol."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Gran\u00e9li, E., and Turner, J.T. (2006). Chemical and physical factors influencing toxin content. Ecology of Harmful Algae, Springer.","DOI":"10.1007\/978-3-540-32210-8"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.hal.2011.12.003","article-title":"Nitrogen and phosphorus limitation effects on cell growth, biovolume, and toxin production in Ostreopsis cf. ovata","volume":"15","author":"Vanucci","year":"2012","journal-title":"Harmful Algae"},{"key":"ref_82","unstructured":"Xu, Z. (2023). Response of Hemolytic Activity in Relation to Photosynthetic System of Chattonella antiqua, Zhejiang University."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1139\/m62-029","article-title":"Studies of marine planktonic diatoms. I. Thalassiosira pseudonana (Cyclotella nana) (Hustedt), and Detonula confervacea (Cleve) Gran","volume":"8","author":"Guillard","year":"1962","journal-title":"Can. J. Microbiol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1705","DOI":"10.1007\/s10811-015-0704-4","article-title":"Marine phytoplankton preservation with Lugol\u2019s: A comparison of solutions","volume":"28","author":"Williams","year":"2016","journal-title":"J. Appl. Phycol."},{"key":"ref_85","unstructured":"Stein, J.R. (1973). Handbook of Phycological Methods: Culture Methods and Growth Measurements, Cambridge University Press."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1016\/j.hal.2010.04.004","article-title":"Expression and standardized measurement of hemolytic activity in Heterosigma akashiwo","volume":"9","author":"Ling","year":"2010","journal-title":"Harmful Algae"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1852","DOI":"10.1111\/nph.19056","article-title":"Regulation of photosynthetic and hemolytic activity of Phaeocystis globosa under different light spectra","volume":"239","author":"Song","year":"2023","journal-title":"New Phytol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1111\/j.1529-8817.2008.00471.x","article-title":"The Role of Reactive Oxygen Species in Copper Toxicity to Two Freshwater Green Algae","volume":"44","author":"Knauert","year":"2008","journal-title":"J. Phycol."}],"container-title":["Toxins"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6651\/18\/5\/226\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,16]],"date-time":"2026-05-16T04:11:06Z","timestamp":1778904666000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6651\/18\/5\/226"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,5,9]]},"references-count":88,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2026,5]]}},"alternative-id":["toxins18050226"],"URL":"https:\/\/doi.org\/10.3390\/toxins18050226","relation":{},"ISSN":["2072-6651"],"issn-type":[{"value":"2072-6651","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,5,9]]}}}