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Superoxide production rates and hemolytic activity linked to cellular growth phases in Chattonella species (Raphidophyceae) and Margalefidinium polykrikoides (Dinophyceae)

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Abstract

The increased occurrence of ichthyotoxic blooms of Chattonella and Margalefidinium species has led to mass fish kills causing multi-million dollar economic losses in diverse marine environments. Their ichthyotoxicity may be driven by a synergistic effect of diverse chemical compounds, of which little is understood in terms of production and biological activity. This study analyzed the growth rates, superoxide radical (O2●−) production rate, lipid peroxidation (TBARS) levels, and hemolytic activity of the ichthyotoxic raphidophytes Chattonella complex (C. var. marina, C. var. ovata, C. var. antiqua), C. subsalsa and the dinoflagellate Margalefidinium polykrikoides. Growth interactions between Chattonella and M. polykrikoides were also analyzed in bi-algal cultures. Chattonella strains exhibited higher growth rates than M. polykrikoides in monocultures. Highest O2●− production rate and TBARS levels in cells occurred in the early exponential growth phase, where M. polykrikoides showed higher values compared with Chattonella strains. Highest hemolytic activity associated to higher cell abundance was caused by M. polykrikoides followed by raphidophytes during the stationary and exponential growth phase, respectively. Of the three Chattonella strains, only C. subsalsa growth was inhibited when grown in bi-algal cultures with M. polykrikoides. In conclusion, this study supports an ecological linkage between cell growth conditions and a dynamic production of O2●− and/or hemolysins, which may mediate its ichthyotoxicity. However, the potential involvement in mass fish kills and ecological implications for local trophic webs remains to be further elucidated.

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References

  • Ahluwalia AS (2013) Cyanobacterial and algal allelopathy. In: Cheema Z, Farooq M, Wahid A (eds) Allelopathy. Springer, Berlin, pp 485–509.

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    CAS  PubMed  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    CAS  PubMed  PubMed Central  Google Scholar 

  • Band-Schmidt CJ, Morquecho-Escamilla ML, Hernández-Becerril DU, Reyes-Salinas A, Bravo-Sierra E (2004) Raphidopyceans in Mexican coasts. Hydrobiologia 515:79–84

    Google Scholar 

  • Band-Schmidt CJ, Martínez-López A, Gárate-Lizárraga I (2005) First record of Chattonella marina in Bahía de La Paz, Gulf of California. Harmful Algae News 28:6–7

    Google Scholar 

  • Band-Schmidt CJ, Martínez-López A, Bustillos-Guzmán JJ, Carréon-Palau L, Morquecho L, Olguín-Monroy NO, Zenteno-Savín T, Mendoza-Flores A, González-Acosta B, Hernández-Sandoval FE, Tomas C (2012) Morphology, biochemistry and growth of Raphidophyte strains from the Gulf of California. Hydrobiologia 693:81–97

    CAS  Google Scholar 

  • Band-Schmidt CJ, Zumaya-Higuera MG, López-Cortés DJ, Leyva-Valencia I, Quijano-Scheggia SI, Hernández-Guerrero CJ (2020) Allelopathic effects of Margalefidinium polykrikoides and Gymnodinium impudicum in the growth of Gymnodinium catenatum. Harmful Algae 96:101846

    CAS  PubMed  Google Scholar 

  • Barraza-Guardado R, Cortes-Altamirano R, Sierra-Beltrán A (2004) Marine die-offs from Chattonella marina and Ch. cf ovata in Kun Kaak Bay, Sonora in the Gulf of California. Harmful Algae News 25:7–8

    Google Scholar 

  • Buettner GR (2011) Superoxide dismutase in redox biology: the roles of superoxide and hydrogen peroxide. Anti Cancer Agents Med Chem 11:341–346

    CAS  Google Scholar 

  • Bustillos-Guzmán JJ, Band-Schmidt CJ, Durán-Riveroll LM, Hernández-Sandoval FE, López-Cortés DJ, Núñez-Vázquez EJ, Cembella A, Krock B (2015) Paralytic toxin profile of the marine dinoflagellate Gymnodinium catenatum (Graham) from the Mexican Pacific as revealed by liquid chromatography coupled with tandem mass spectrometry. Food Addit Contam A:1–14.

  • Cho K, Kasaoka T, Ueno M, Basti L, Yamasaki Y, Kim D, Oda T (2017) Haemolytic activity and reactive oxygen species production of four harmful algal bloom species. Eur J Phycol 52:311–319

    CAS  Google Scholar 

  • Cirulis JT, Scott JA, Ross GM (2013) Management of oxidative stress by microalgae. Can J Physiol Pharm 91:15–21

    CAS  Google Scholar 

  • Cortés-Altamirano R, Alonso-Rodríguez R, Sierra-Beltrán A (2006) Fish mortality associated with Chattonella and C. cf ovata (Raphidophyceae) blooms in Sinaloa (Mexico). Harmful Algae News 7-8:31

    Google Scholar 

  • Demura M, Noel MH, Kasai F, Watanabe MM, Kawachi M (2009) Taxonomic revision of Chattonella antiqua, C. marina and C. ovata (Raphidophyceae) based on their morphological characteristics and genetic diversity. Phycologia 48:518–535

    Google Scholar 

  • Diaz JM, Plummer S (2018) Production of extracellular reactive oxygen species by phytoplankton: past and future directions. J Plankton Res 0:1–12.

  • Diaz JM, Plummer S, Tomas C, Alves-de Souza C (2018) Production of extracellular superoxide and hydrogen peroxide by five marine species of harmful bloom-forming algae. J Plankton Res 40:667–677

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dorantes-Aranda JJ, Nichols PD, Waite TD, Hallegraeff GM (2013) Strain variability in fatty acid composition of Chattonella marina (Raphidophyceae) and its relation to differing ichthyotoxicity toward rainbow trout gill cells. J Phycol 49:427–438

    CAS  PubMed  Google Scholar 

  • Dorantes-Aranda JJ, Seger A, Mardones JI, Nichols PD, Hallegraeff GM (2015) Progress in understanding algal bloom-mediated fish kills: the role of superoxide radicals, phycotoxins and fatty acids. PLoS One 10:e0133549

    PubMed  PubMed Central  Google Scholar 

  • Drossos G, Lazou A, Panagopoulos P, Westaby S (1995) Deferoxamine cardioplegia reduces superoxide radical production in human myocardium. Ann Thorac Surg 59:169–172

    CAS  PubMed  Google Scholar 

  • Eilola K, Almroth E, Naustvoll LJ, Andersson P, Karlson B (2006) Modelling the dynamics of harmful blooms of Chattonella sp. in the Skagerrak and the Kattegat. ICES CM 2006/E12, ICES Annual Science Conference

  • Eschbach E, Scharsack JP, John U, Medlin LK (2001) Improved erythrocyte lysis assay in microtitre plates for sensitive detection and efficient measurement of haemolytic compounds from ichthyotoxic alga. J Appl Toxicol 21:513–519

    CAS  PubMed  Google Scholar 

  • Fernández-Herrera LJ, Band-Schmidt CJ, López-Cortés DJ, Hernández-Guerrero CJ, Bustillos-Guzmán JJ, Núñez-Vázquez EJ (2016) Allelopathic effect of Chattonella marina var. marina (Raphidophyceae) on Gymnodinium catenatum (Dinophycea). Harmful Algae 51:1–9

    PubMed  Google Scholar 

  • Flood SL, Burkholder JM (2018) Chattonella subsalsa (Raphidophyceae) growth and hemolytic activity in response to agriculturally-derived estuarine contaminants. Harmful Algae 76:66–79

    CAS  PubMed  Google Scholar 

  • Gárate-Lizárraga I (2013) Bloom of Cochlodinium polykrikoides (Dinophyceae: Gymnodiniales) in Bahía de La Paz, Gulf of California. Mar Pollut Bull 67:217–222

    PubMed  Google Scholar 

  • Gárate-Lizárraga I, Bustillos-Guzmán JJ, Morquecho LM, Lechuga-Devéze CH (2000) First outbreak of Cochlodinium polykrikoides in the Gulf of California. Harmful Algae News 21:7

    Google Scholar 

  • Gárate-Lizárraga I, López-Cortes DJ, Bustillos-Guzmán JJ, Hernández-Sandoval F (2004) Blooms of Cochlodinium polykrikoides (Gymnodiniaceae) in the Gulf of California, Mexico. Rev Biol Tropical 52:51–58

    Google Scholar 

  • Gárate-Lizárraga I, Band-Schmidt CJ, Aguirre-Bahena F, Grayeb-del-Alamo T (2009a) A multi-species microalgae bloom in Bahía de La Paz, Gulf of California, Mexico (June 2008). CICIMAR Oceánides 24:15–29

    Google Scholar 

  • Gárate-Lizárraga I, Díaz-Ortiz J, Pérez-Cruz B, Alarcón-Tacuba M, Torres-Jaramillo A, Alarcón-Romero MA, López-Silva S (2009b) Cochlodinium polykrikoides and Gymnodinium catenatum in Bahía de Acapulco, Mexico (2005-2008). Harmful Algae News 40:8–9

    Google Scholar 

  • García-Mendoza E, Cáceres-Martínez J, Rivas D, Fimbres-Martínez M, Sánchez-Bravo Y, Vásquez-Yeomans R, 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 5:454

    Google Scholar 

  • Gómez F, Richlen ML, Anderson DM (2017) Molecular characterization and morphology of Cochlodinium strangulatum, the type species of Cochlodinium, and Margalefidinium gen. nov for C. polykrikoides and allied species (Gymnodiniales, Dinophyceae). Harmful Algae 63:32–44

    PubMed  PubMed Central  Google Scholar 

  • Imai I, Yamaguchi M (2012) Life cycle, physiology, ecology and red tide occurrences of the fish-killing raphidophyte Chattonella. Harmful Algae 14:46–70

    Google Scholar 

  • Ishimatsu A, Oda T, Yoshida M, Ozaki M (1996) Oxygen radicals are probably involved in the mortality of yellowtail by Chattonella marina. Fish Sci 62:836–837

    CAS  Google Scholar 

  • Jeffrey SW, Vesk M (1997) Introduction to marine phytoplankton and their pigment signatures. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography: guidelines to modern methods, monographs on oceanographic methodology. SCOR-UNESCO, Paris, pp 37–84

    Google Scholar 

  • Jeong HJ (2011) Mixotrophy in red tide algae Raphidophytes. J Eukaryot Microbiol 58:215–222

    PubMed  Google Scholar 

  • Jeong HJ, Yoo YD, Kim JS, Kim TH, Kim JH, Kang NS, Yih W (2004) Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dinophyceae); prey species, the effects of prey concentration, and grazing impact. J Eukaryot Microbiol 51:563–569

    PubMed  Google Scholar 

  • Katano T, Yoshida M, Lee J, Han M-S, Hayami Y (2009) Fixation of Chattonella antiqua and C. marina (Raphidophyceae) using Hepes-buffered paraformaldehyde and glutaraldehyde for flow cytometry and light microscopy. Phycologia 48:473–479

    Google Scholar 

  • Kawano I, Oda T, Ishimatsu A, Muramatsu T (1996) Inhibitory effect of the iron chelator Desferrioxamine (Desferal) on the generation of activated oxygen species by Chattonella marina. Mar Biol 126:765–771

    CAS  Google Scholar 

  • Kim D, Oda T (2014) Production of nitric oxide by marine unicellular red tide phytoplankton Chattonella marina. In: Khan MN, Mobin M, Mohammad F, Corpas FJ (eds) Nitric oxide in plants: metabolism and role in stress physiology. Springer, Cham, pp 75–84.

  • Kim CS, Lee SG, Lee CK, Kim HG, Jung J (1999a) Reactive oxygen species as causative agents in the ichthyotoxicity of the red tide dinoflagellate Cochlodinium polykrikoides. J Plankton Res 21:2105–2115

    CAS  Google Scholar 

  • Kim D, Oda T, Ishimatsu A, Muramatsu T (1999b) Isolation and characterization of a mutant strain of Chattonella marina with decreased production of superoxide anion. Biosci Biotechnol Biochem 63:1947–1952

    CAS  Google Scholar 

  • Kim CS, Lee SG, Kim HG (2000) Biochemical responses of fish exposed to a harmful dinoflagellate Cochlodinium polykrikoides. J Exp Mar Biol Ecol 254:131–141

    CAS  PubMed  Google Scholar 

  • Kim D, Oda T, Maramatsu T, Kim D, Matsuyama Y, Honjo T (2002) Possible factors responsible for the toxicity of Cochlodinium polykrikoides, a red tide phytoplankton. Comp Biochem Physiol C 132:145–423

    Google Scholar 

  • Kim D-I, Matsuyama Y, Nagasoe S, Yamaguchi M, Yoon Y-H, Oshima Y, Imada N, Honjo T (2004) Effects of temperature, salinity and irradiance on the growth of the harmful red tide dinoflagellate Cochlodinium polykrikoides Margalef (Dinophyceae). J Plankton Res 26:61–66

    Google Scholar 

  • Kim D, Nakashima T, Matsuyama Y, Niwano Y, Yamaguchi K, Oda T (2007) Presence of the distinct systems responsible for superoxide anion and hydrogen peroxide generation in red tide phytoplankton Chattonella marina and Chattonella ovata. J Plankton Res 29:241–247

    CAS  Google Scholar 

  • Kim D, Kang YS, Lee Y, Yamaguchi K, Matsuoka K, Lee K-W, Choi K-S, Oda T (2008) Detection of nitric oxide (NO) in marine phytoplankters. J Biosci Bioeng 105:414–417

    CAS  PubMed  Google Scholar 

  • Klöpper S, John U, Zingone A, Mangoni O, Kooistra WHCF, Cembella AD (2013) Phylogeny and morphology of a Chattonella (Raphidophyceae) species from the Mediterranean Sea: what is C. subsalsa? Eur J Phycol 48:79–92

    Google Scholar 

  • Kudela RM, Gobler CJ (2012) Harmful dinoflagellate blooms caused by Cochlodinium sp.: global expansion and ecological strategies facilitating bloom formation. Harmful Algae 14:71–86

    Google Scholar 

  • Kudela RM, Ryan JP, Blakely MD, Lane JQ, Peterson TD (2008) Linking the physiology and ecology of Cochlodinium to better understand algal bloom events: a comparative approach. Harmful Algae 7:278–292

    CAS  Google Scholar 

  • Kuroda A, Nakashima T, Yamaguchi K, Oda T (2005) Isolation and characterization of light-dependent hemolytic cytotoxin from harmful red tide phytoplankton Chattonella marina. Comp Biochem Physiol C 141:297–305

    Google Scholar 

  • Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113–390

    Google Scholar 

  • Li X, Liu T, Wang K, Waite D (2015) Light-induced extracellular electron transport by the marine raphidophyte Chattonella marina. Environ Sci Technol 49:1392–1399

    CAS  PubMed  Google Scholar 

  • Lim AS, Jeong HJ, Jang TY, Jang SH, Franks PJS (2014) Inhibition of growth rate and swimming speed of the harmful dinoflagellate Cochlodinium polykrikoides by diatoms: implications for red tide formation. Harmful Algae 37:53–61

    Google Scholar 

  • Liu W, Au DWT, Anderson DM, Lam PKS, Wu RSS (2007) Effects of nutrients, salinity, pH and light:dark cycle on the production of reactive oxygen species in the alga Chattonella marina. J Exp Mar Biol Ecol 346:76–86

    CAS  Google Scholar 

  • López-Cortés DJ, Band-Schmidt CJ, Gárate-Lizárraga I, Bustillos-Guzmán JJ, Hernández-Sandoval FE, Núñez-Vázquez EJ (2011) Co-ocurrencia de Chattonella marina y Gymnodinium catenatum en la Bahía de La Paz, Golfo de California (primavera 2009). Hidrobiológica 21:185–196

    Google Scholar 

  • López-Cortés DJ, Band-Schmidt CJ, Bustillos-Guzmán JJ, Hernández-Sandoval FE, Mendoza-Flores A, Núñez-Vázquez EJ (2014) Condiciones ambientales durante un florecimiento de Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae) en la Ensenada de La Paz, Golfo de California. Rev Biol Mar Oceanogr 49:97–110

    Google Scholar 

  • López-Cortés D, Núñez-Vázquez E, Dorantes-Aranda J, Band-Schmidt C, Hernández-Sandoval F, Bustillos-Guzmán J, Leyva-Valencia I, Fernández-Herrera L (2019) The state of knowledge of harmful algal blooms of Cochlodinium polykrikoides in Latin America. Front Mar Sci 6:463

    Google Scholar 

  • Marshall JA, Hallegraeff GM (1999) Comparative ecophysiology of the harmful alga Chattonella marina (Raphidophyceae) from south Australian and Japanese waters. J Plankton Res 21:1809–1822

    Google Scholar 

  • Marshall JA, Hovenden M, Oda T, Hallegraeff GM (2002) Photosynthesis does influence superoxide production in the ichthyotoxic alga Chattonella marina (Raphidophyceae). J Plankton Res 24:1231–1236

    CAS  Google Scholar 

  • Marshall JA, Nichols PD, Hamilton B, Lewis RJ, Hallegraeff GM (2003) Ichthyotoxicity of Chattonella marina (Raphidophyceae) to damselfish (Acanthochromis polycanthus): the synergistic role of reactive oxygen species and free fatty acids. Harmful Algae 2:273–281

    CAS  Google Scholar 

  • Marshall JA, Ross T, Pyecroft S, Hallegraeff G (2005) Superoxide production by marine microalgae - II. Towards understanding ecological consequences and possible functions. Mar Biol 147:541–549

    CAS  Google Scholar 

  • Meave-del-Castillo ME, Zamudio-Resendiz ME (2018) Planktonic algal blooms from 2000 to 2015 in Acapulco Bay, Guerrero, Mexico. Acta Bot Mex 125:61–93

    Google Scholar 

  • Mulholland MR, Morse RE, Boneillo GE, Bernhardt PW, Filippino KC, Procise LA, Blanco-Garcia JL, Marshall HG, Egerton TA, Hunley WS, Moore KA, Berry DL, Gobler CJ (2009) Understanding causes and impacts of the dinoflagellate, Cochlodinium polykrikoides, blooms in the Chesapeake Bay. Estuar Coast 32:734–747

    CAS  Google Scholar 

  • Munné-Bosch S, Pintó-Marijuan M (2017) Free radicals, oxidative stress and antioxidants. In: Thomas B, Murphy DJ, Murray BG (eds) Encyclopedia of applied plant sciences. Academic Press, New York, pp 16–19

    Google Scholar 

  • Muñoz P, Munné-Bosch S (2018) Photo-oxidative stress during leaf, flower and fruit development. Plant Physiol 176:1004–1014

    PubMed  Google Scholar 

  • Nakamura Y (1985) Kinetics of nitrogen- or phosphorus-limited growth and effects of growth conditions on nutrient uptake in Chattonella antiqua. J Oceanogr Soc Jpn 41:381–387

    CAS  Google Scholar 

  • Nakamura Y, Watanabe M (1983) Growth characteristics of Chattonella antiqua (Raphidophyceae). Part 1. Effect of temperature, salinity, light intensity and pH on growth. J Oceanogr Soc Jpn 39:110–114

    Google Scholar 

  • Oda T, Akaike T, Sato K, Ishimatsu A, Takeshita S, Maramatsu T, Maeda H (1992) Hydroxyl radical generation by red tide algae. Arch Biochem Biophys 294:38–43

    CAS  PubMed  Google Scholar 

  • Oda T, Ishimatsu A, Takeshita S, Muramatsu T (1994) Hydrogen-peroxide production by the red-tide flagellate Chattonella marina. Biosci Biotechnol Biochem 58:957–958

    CAS  Google Scholar 

  • Oda T, Moritomi J, Kawano I, Hamaguchi S, Ishimatsu A, Muramatsu T (1995) Catalase-induced and superoxide dismutase induced morphological changes and growth-inhibition in the red tide phytoplankton Chattonella marina. Biosci Biotechnol Biochem 59:2044–2048

    CAS  Google Scholar 

  • Oda T, Nakamura A, Shikayama M, Kawano I, Ishimatsu A, Muramatsu T (1997) Generation of reactive oxygen species by raphidophycean phytoplankton. Biosci Biotechnol Biochem 61:1658–1662

    CAS  PubMed  Google Scholar 

  • Oh SJ, Yoo YH, Kim D-I, Shimasaki Y, Oshima Y, Honjo T (2006) Effects of light quantity and quality on the growth of the harmful dinoflagellate, Cochlodinium polykrikoides Margalef (Dinophycea). Algae 21:311–316

    Google Scholar 

  • Pérez-Morales A, Band-Schmidt CJ, Ortíz-Galindo JL, Sobrino-Figueroa AS (2014) Mortality in the initial ontogeny of Paralabrax maculatofasciatus (Serranidae) (Actinopterygii, Perciformes) caused by Chattonella spp. (Raphidophyceae). Hydrobiologia 722:247–261

    Google Scholar 

  • Pérez-Morales A, Band-Schmidt CJ, Martínez-Díaz SF (2017) Mortality on zoea stage of the Pacific white shrimp Litopenaeus vannamei caused by Cochlodinium polykrikoides (Dinophyceae) and Chattonella spp. (Raphidophyceae). Mar Biol 164:57

    Google Scholar 

  • Persky AM, Green PS, Stubley LC, Howell O, Zaulyanov L, Brzaeau GA, Simpkins JW (2000) Protective effect of estrogens against oxidative damage to heart and skeletal muscle in vivo and in vitro. Proc Soc Exp Biol Med 223:59–66

    CAS  PubMed  Google Scholar 

  • Pintó-Marijuan M, Munné-Bosch S (2014) Photo-oxidative stress markers as a measure of abiotic stress-induced leaf senescence: advantages and limitations. J Exp Bot 65:3845–3857

    PubMed  Google Scholar 

  • Pospíšil P (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta 1817:218–231

    PubMed  Google Scholar 

  • Qiu X, Yamasaki Y, Shimasaki Y, Gunjikake H, Matsubara T, Nagasoe S, Etoh T, Matsui S, Honjo T, Oshima Y (2011a) Growth interactions between the raphidophyte Chattonella antiqua and the dinoflagellate Akashiwo sanguinea. Harmful Algae 11:81–87

    Google Scholar 

  • Qiu X, Yamasaki Y, Shimasaki Y, Gunjikake H, Shikata T, Matsubara T, Nagasoe S, Etoh T, Matsui S, Honjo T, Oshima Y (2011b) Growth interactions between raphidophytes Chattonella antiqua and Heterosigma akashiwo. Thalassas 27:33–45

    Google Scholar 

  • Raven JA, Griffiths H (2015) Photosynthesis in reproductive structures: costs and benefits. J Exp Bot 66:1699–1705

    CAS  PubMed  PubMed Central  Google Scholar 

  • Satta CT, Padedda BM, Sechi N, Pulina S, Loria A, Lugliè A (2017) Multiannual Chattonella subsalsa Biecheler (Raphidophyceae) blooms in a Mediterranean lagoon (Santa Giusta Lagoon, Sardinia Island, Italy). Harmful Algae 67:61–73

    PubMed  Google Scholar 

  • Shahraki J, Motallebi A, Pourahmad J (2013) Oxidative mechanisms of fish hepatocyte toxicity by the harmful dinoflagellate Cochlodinium polykrikoides. Mar Environ Res 87-88:52–60

    CAS  PubMed  Google Scholar 

  • Shi K, Gao Z, Shi TQ, Song P, Ren LJ, Huang H, Ji XJ (2017) Reactive oxygen species-mediated cellular stress response and lipid accumulation in oleaginous microorganisms: the state of the art and future perspectives. Front Microbiol 8:793

    PubMed  PubMed Central  Google Scholar 

  • Tang YZ, Gobler CJ (2009a) Characterization of the toxicity of Cochlodinium polykrikoides isolates from northeast US estuaries to finfish and shellfish. Harmful Algae 8:454–462

    CAS  Google Scholar 

  • Tang YZ, Gobler CJ (2009b) Cochlodinium polykrikoides blooms and clonal isolates from the northwest Atlantic coast cause rapid mortality in larvae of multiple bivalve species. Mar Biol 156:2601–2611

    CAS  Google Scholar 

  • Tang YZ, Gobler CJ (2010) Allelopathic effects of Cochlodinium polykrikoides isolates and blooms from the estuaries of Long Island, New York, on co-occurring phytoplankton. Mar Ecol Prog Ser 406:19–31

    Google Scholar 

  • Tiffany MA, Barlow SB, Matey VE, Hurlbert SH (2001) Chattonella marina (Raphidophyceae), a potentially toxic alga in the Salton Sea, California. Hydrobiologia 466:187–194

    Google Scholar 

  • Tilney CL, Hoadley KD, Warner ME (2015) Comparing the diel vertical migration of Karlodinium veneficum (Dinophyceae) and Chattonella subsalsa (Raphidophyceae): PSII photochemistry, circadian control, and carbon assimilation. J Photochem Photobiol B 143:107–119

    CAS  PubMed  Google Scholar 

  • Tomas CR, Ono C, Yoshimatsu S, Göbel J (2004) Chattonella verrucolosa and related species from Japan, Europe (North Sea) and US coastal waters: cases of mistaken identity? In: Steidinger KA, Landsberg JH, Tomas CR, Vargo GA (eds) Harmful Algae 2002. Florida Fish and Wildlife Conservation Commission and Intergovernmental Oceanographic Commission of UNESCO, Florida, pp 425–427

    Google Scholar 

  • Viana TV, Fistarol GO, Amario M, Menezes RB, Carneiro BLR, Chaves DM, Hargreaves PI, Silva-Lima AW, Valentin JL, Tenenbaum DR, Arruda EF, Paranhos R, Salomon PS (2019) Massive blooms of Chattonella subsalsa Biecheler (Raphidophyceae) in a hypereutrophic, tropical estuary-Guanabara Bay, Brazil. Front Mar Sci 6:85

    Google Scholar 

  • Watanabe M, Kohata K, Kimura T, Yamaguchi S-I, Ioriya T (1995) Generation of a Chattonella antiqua bloom by imposing a shallow nutricline in a mesocosm. Limnol Oceanogr 40:1447–1460

    Google Scholar 

  • Wood AM, Everroad RC, Wingard LM (2005) Measuring growth rates in microalgal cultures. In: Andersen RA (ed) Algal culturing techniques. Elsevier, Amsterdam, pp 269–285.

  • Wu J-T, Chiang YR, Huang W-Y, Jane W-N (2006) Cytotoxic effect of free fatty acids on phytoplankton algae and cyanobacteria. Aquat Toxicol 80:338–345

    CAS  PubMed  Google Scholar 

  • Yamaguchi H, Sakamoto S, Yamaguchi M (2008) Nutrition and growth kinetics in nitrogen- and phosphorus-limited cultures of the novel red tide flagellate Chattonella ovata (Raphidophyceae). Harmful Algae 7:26–32

    CAS  Google Scholar 

  • Yamaguchi H, Mizushima K, Sakamoto S, Yamaguchi M (2010) Effects of temperature, salinity and irradiance on growth of the novel red tide flagellate Chattonella ovata (Raphidophyceae). Harmful Algae 9:398–401

    Google Scholar 

  • 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. Mar Biol 152:157–163

    Google Scholar 

  • Yamatogi T, Sakaguchi M, Takagi N, Iwataki M, Matsuoka K (2005) Effects of temperature, salinity and light intensity on the growth of a harmful dinoflagellate Cochlodinium polykrikoides Margalef occurring in coastal waters of West Kyushu, Japan. Bull Plankton Soc Japan 52:4–10

    Google Scholar 

  • Yamatogi T, Sakaguchi M, Iwataki M, Matsuoka K (2006) Effects of temperature and salinity on the growth of four harmful red tide flagellates occurring in Isahaya Bay in Ariake Sound, Japan. Nippon Suisan Gakk 72:160–168

    Google Scholar 

  • Zhang YH, Fu FX, Whereat E, Coyne KJ, Hutchins DA (2006) 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. Harmful Algae 5:310–320

    CAS  Google Scholar 

  • Zhaohui W, Meiling Y, Yu L, Songhui L (2011) Effects of temperature and organic and inorganic nutrients on the growth of Chattonella marina (Raphidophyceae) from the Daya Bay, South China Sea. Acta Oceanol Sin 30:124–131

    Google Scholar 

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Acknowledgments

Authors gratefully acknowledge O. Lugo-Lugo and N.O. Olguín-Monroy for their assistance in sample analyses at the Laboratory of Oxidative Stress at the Centro de Investigaciones Biológicas del Noroeste (CIBNOR), S.C. CJB-S is a recipient of an EDI and a COFAA fellowship.

Funding

This work was supported by the Consejo Nacional de Ciencia y Tecnología (CONACyT) of Mexico through a postdoctoral scholarship to AA-C. Research was supported by the projects SEP-CONACyT 178227 and SAPPI 2020–0571 granted to CJB-S, and the institutional projects PC2.0, PC0.10, and PC0.5 of the Centro de Investigaciones Biológicas del Noroeste (CIBNOR), S.C.

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Correspondence to A. Aquino-Cruz.

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Aquino-Cruz, A., Band-Schmidt, C.J. & Zenteno-Savín, T. Superoxide production rates and hemolytic activity linked to cellular growth phases in Chattonella species (Raphidophyceae) and Margalefidinium polykrikoides (Dinophyceae). J Appl Phycol 32, 4029–4046 (2020). https://doi.org/10.1007/s10811-020-02218-w

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