Effect of a bacterial consortium on the growth, morphology, pigments, and toxicity of the dinoflagellate Gymnodinium catenatum
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Abstract
Gymnodinium catenatum, a dinoflagellate that produces paralytic toxins, is one of the most studied dinoflagellate species. However, scarce information exists about its interaction with bacteria. In this study, the effect of a bacterial consortium in strains of G. catenatum was determined. Four strains of G. catenatum isolated from Bahía de Santiago, Colima; Lázaro Cárdenas, Michoacán; and Bahía Concepción and Bahía de La Paz, Baja California Sur were used. From the strain isolated from the coasts of Colima, a bacterial consortium was isolated with agar plates with GSe media that were incubated at a salinity of 34, at 24 °C in a L:D cycle of 12:12 h. Gymnodinum catenatum was cultivated in GSe media under the same conditions as the bacterial consortium. The interaction between these microorganisms was evaluated inoculating G. catenatum strains with the bacterial consortium. The maximum abundance, growth rate, chain length, toxin, and pigment profile were determined in G. catenatum with and without the bacterial consortium. In the presence of bacteria there was no clear effect on the growth, toxin profile, and toxin content in G. catenatum, but a significant increase in the chain length was observed. Changes in cell morphology were also observed. In addition, in the presence of the bacterial consortium, there was an increase in accessory pigments in most strains. Results suggest that the bacterial consortium could be a stress factor for G. catenatum and provide new perspectives on the interaction between bacteria and G. catenatum.
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Alavi M, Miller T, Erlandson K, Schneider R, Belas R. 2001. Bacterial community associated with Pfiesteria-like dinoflagellate cultures. Environ Microbiol. 3:380-396. https://doi.org/10.1046/j.1462-2920.2001.0 DOI: https://doi.org/10.1046/j.1462-2920.2001.00207.x
Albinsson ME, Negri AP, Blackburn SI, Bolch CJS. 2014. Bacterial community affects toxin production by Gymnodinium catenatum. PLoS ONE. 9:e104623. https://doi.org/10.1371/journal.pone.0104623 DOI: https://doi.org/10.1371/journal.pone.0104623
Alonso-Rodríguez R, Páez-Osuna F. 2003. Nutrients, phytoplankton and harmful algal blooms in shrimp ponds: a review with special reference to the situation in the Gulf of California. Aquaculture. 219:317-336. https://doi.org/10.1016/S0044-8486(02)00509-4 DOI: https://doi.org/10.1016/S0044-8486(02)00509-4
Amin S, Küpper FC, Green DH, Harris WR, Carrano CJ. 2007. Boron binding by a siderophore isolated from marine bacteria associated with the toxic dinoflagellate Gymnodinium catenatum. J Am Chem Soc. 129:478-479. https://doi.org/10.1021/ja067369u DOI: https://doi.org/10.1021/ja067369u
Azam F. 1998. Microbial control of oceanic carbon flux: the plot thickens. Science. 280:694-696. DOI: https://doi.org/10.1126/science.280.5364.694
Band-Schmidt CJ, Bustillos-Guzmán J, Gárate-Lizárraga I, Lechuga-Devéze CH, Reinhardt K, Luckas B. 2005. Paralytic shellfish toxin profile in strains of the dinoflagellate Gymnodinium catenatum Graham and the scallop Argopecten ventricosus G.B. Sowerby II from Bahía Concepción, Gulf of California, Mexico. Harmful Algae. 4(1):21-31. https://doi.org/10.1016/j.hal.2003.10.004 DOI: https://doi.org/10.1016/j.hal.2003.10.004
Band-Schmidt CJ, Bustillos-Guzmán JJ, Hernández-Sandoval FE, Núñez-Vázquez EJ, López-Cortés DJ. 2014. Effect of temperature on growth and paralytic toxin profiles in isolates of Gymnodinium catenatum (Dinophyceae) of the Pacific coast of Mexico. Toxicon. 90:199-212. https://doi.org/10.1016/j.toxicon.2014.08.002 DOI: https://doi.org/10.1016/j.toxicon.2014.08.002
Band-Schmidt CJ, Bustillos-Guzmán JJ, López-Cortés DJ, Gárate-Lizárraga I, Núñez-Vázquez E, Hernández-Sandoval, FE. 2010. Ecological and physiological studies of Gymnodinium catenatum in the Mexican Pacific: a review. Mar Drugs. 8:1935-1961. https://doi.org/10.3390/md8061935 DOI: https://doi.org/10.3390/md8061935
Band-Schmidt CJ, Bustillos-Guzmán JJ, Morquecho L, Gárate-Lizárraga I, Alonso-Rodríguez R, Reyes-Salinas A, Erler K, Luckas B. 2006. Variations of PSP toxin profiles during different growth phases in Gymnodinium catenatum (Dinophyceae) strains isolated from three locations in the Gulf of California, Mexico. J Phycol. 42:757-768. https://doi.org/10.1111/j.1529-8817.2006.00234.x DOI: https://doi.org/10.1111/j.1529-8817.2006.00234.x
Band-Schmidt CJ, Durán-Riveroll LM, Bustillos-Guzmán JJ, López-Cortés DJ, Núñez-Vázquez EJ, Hernández-Sandoval FE, Ramírez-Rodríguez DV. 2019. Paralytic toxin producing dinoflagellates in Latin America: Ecology and Physiology (a review). Front Mar Sci. 6:42. https://doi.org/10.3389/fmars.2019.00042 DOI: https://doi.org/10.3389/fmars.2019.00042
Band-Schmidt CJ, Morquecho L, Lechuga-Devéze CH, Anderson DM. 2004. Effects of growth medium, temperature, salinity and seawater source on the growth of Gymnodinium catenatum (Dinophyceae) from Bahía Concepción, Gulf of California, Mexico. J Plankton Res. 26:1459-1470. https://doi.org/10.1093/plankt/fbh133 DOI: https://doi.org/10.1093/plankt/fbh133
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. https://doi.org/10.1016/j.hal.2020.101846 DOI: https://doi.org/10.1016/j.hal.2020.101846
Blackburn SI, Bolch CJS, Haskard KA, Hallegraeff GM. 2001. Reproductive compatibility among four global populations of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae). Phycol. 40:78-87. https://doi.org/10.2216/i0031-8884-40-1-78.1 DOI: https://doi.org/10.2216/i0031-8884-40-1-78.1
Blackburn SI, Hallegraeff GM, Bolch CJ. 1989. Vegetative reproduction and sexual life cycle of the toxic dinoflagellate Gymnodinium catenatum from Tasmania, Australia. J Phycol. 25:577-590. https://doi.org/10.1111/j.1529-8817.1989.tb00264.x DOI: https://doi.org/10.1111/j.1529-8817.1989.tb00264.x
Bolch CJS, Bejoy TA, Green DH. 2017. Bacterial associates modify growth dynamics of the dinoflagellate Gymnodinium catenatum. Front Microbiol. 8:670. https://doi.org/10.3389/fmicb.2017.00670 DOI: https://doi.org/10.3389/fmicb.2017.00670
Bolch CJ, Subramanian TA, Green HG. 2011. The toxic dinoflagellate Gymnodinium catenatum (Dinophyceae) requires marine bacteria for growth. J Phycol. 47:1009-1022. https://doi.org/10.1111/j.1529-8817.2011.01043.x DOI: https://doi.org/10.1111/j.1529-8817.2011.01043.x
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 LC-MS/MS. Food Addit Contam Part A. 32:1-15. https://doi.org/10.1080/19440049.2014.1000978 DOI: https://doi.org/10.1080/19440049.2014.1000978
Bustillos-Guzmán JJ, Band-Schmidt CJ, López-Cortés DJ, Gárate-Lizárraga I, Núñez-Vázquez EJ, Hernández-Sandoval FE. 2012. Variaciones en el crecimiento y toxicidad en Gymnodinium catenatum Graham del Golfo de California bajo diferentes proporciones de nitrógeno y fósforo. Cienc Mar. 38:101-117. DOI: https://doi.org/10.7773/cm.v38i1A.1916
Bustillos-Guzmán JJ, Band-Schmidt CJ, López-Cortés DJ, Hernández-Sandoval FE, Núñez-Vázquez E, Gárate-Lizárraga I. 2013. Pastoreo del dinoflagelado Noctiluca scintillans sobre el dinoflagelado productor de toxinas paralizantes Gymnodinium catenatum: ¿Elimina el pastoreo células durante un florecimiento? Cienc Mar. 39:291-302. DOI: https://doi.org/10.7773/cm.v39i3.2242
Cembella A, Band-Schmidt CJ. 2018. Gymnodinium catenatum. Harmful algal species fact sheets. In: Shumway SE, Burkholder JM, Morton SL (eds.), Harmful Algal Blooms: A compendium desk reference. Hoboken (NJ): Wiley Blackwell. p. 605-611. DOI: https://doi.org/10.1002/9781118994672.ch16k
Chen H. 2018. Emergency treatment and reflection of red tide event of Gymnodinium catenatum in Fujian Sea area in 2017. J Fisheries Res. 40(4):308-314.
Cortés-Altamirano R, Alonso-Rodríguez R, Salas-de-León DA. 2019. Historical observations of algal blooms in Mazatlan Bay, Sinaloa, Mexico (1979-2014). PLoS ONE. 14(1):e0210631. https://doi.org/10.1371/journal.pone.0210631 DOI: https://doi.org/10.1371/journal.pone.0210631
Day RW, Quinn GP. 1989. Comparisons of treatments after an analysis of variance in ecology. Ecol Mon. 59(4):433-463. https://doi.org/10.2307/1943075 DOI: https://doi.org/10.2307/1943075
Durán-Riveroll L, Krock B, Cembella A, Peralta-Cruz J, Bustillos-Guzmán JJ, Band-Schmidt CJ. 2017. Characterization of benzoyl saxitoxin analogs from the toxigenic marine dinoflagellate Gymnodinium catenatum by hydrophilic interaction liquid ion chromatography-tandem mass spectrometry. Nat Prod Chem Res. 5:275. DOI: https://doi.org/10.4172/2329-6836.1000275
Fernández-Herrera LJ, Band-Schmidt CJ, López-Cortés DJ, Hernández-Guerrero CJ, Bustillos-Guzmán JJ, Núñez-Vázquez E. 2016. Allelopathic effect of Chattonella marina var. marina (Raphidophyceae) on Gymnodinium catenatum (Dinophycea). Harmful Algae. 51:1-9. https://doi.org/10.1016/j.hal.2015.10.009 DOI: https://doi.org/10.1016/j.hal.2015.10.009
Fernández-Herrera LJ, Band-Schmidt, CJ, Zenteno-Savín T, Leyva-Valencia I, Hernández-Guerrero CJ, Hernández-Sandoval FE, Bustillos-Guzmán JJ. 2022. Changes in toxin production, morphology and viability of Gymnodinium catenatum associated to allelopathy of Chattonella marina var. marina and Gymnodinium impudicum. Toxins. 14:616. https://doi.org/10.3390/toxins14090616 DOI: https://doi.org/10.3390/toxins14090616
Fernández-Herrera LJ, Band-Schmidt CJ, Zenteno-Savín T, Leyva-Valencia I, Hernández-Guerrero CJ, Muñoz-Ochoa M. 2021. Cell death and metabolic stress in Gymnodinium catenatum induced by allelopathy. Toxins. 13:506. https://doi.org/10.3390/toxins13070506 DOI: https://doi.org/10.3390/toxins13070506
Figueroa RI, Bravo I, Ramilo I, Pazos Y, Moroño A. 2008. New life-cycle stages of Gymnodinium catenatum (Dinophyceae): laboratory and field observations. Aquat Microb Ecol. 52:13-23. https://doi.org/10.3354/ame01206 DOI: https://doi.org/10.3354/ame01206
Figueroa RI, Garcés E, Ramilo I. 2006. Nuclear features and effect of nutrients on Gymnodinium catenatum (Dinophyceae) sexual stages. J Phycol. 42:67-77. https://doi.org/10.1111/j.1529-8817.2006.00181.x DOI: https://doi.org/10.1111/j.1529-8817.2006.00181.x
Fraga S, Gallagher SM, Anderson DM. 1989. Chain-forming dinoflagellates: an adaptation to red tides. In: Okaichi T, Anderson DM, Nemoto T (eds.), Red Tides: Biology, Environmental Science and Toxicology. New York (NY): Elsevier. p. 281-284
Gárate-Lizárraga I, Bustillos-Guzmán JJ, López-Cortés DJ, Hernández-Sandoval F, Erler K, Luckas B. 2006. Paralytic shellfish toxin profiles in net phytoplankton samples from Bahía Concepción, Gulf of California, Mexico. Mar Poll Bull. 52:800-815. https://doi.org/10.1016/j.marpolbul.2006.03.003 DOI: https://doi.org/10.1016/j.marpolbul.2006.03.003
Green DH, Hart MC, Blackburn SI, Bolch CJS. 2010. Bacterial diversity of Gymnodinium catenatum and its relationship to dinoflagellate toxicity. Aquat Microb Ecol. 61:73-87. https://doi.org/10.3354/ame01437 DOI: https://doi.org/10.3354/ame01437
Green DH, Llewellyn LE, Negri AP, Blackburn SI, Bolch CJ. 2004. Phylogenetic and functional diversity of the cultivable bacterial community associated with the paralytic shellfish poisoning dinoflagellate Gymnodinium catenatum. FEMS Microb Ecol. 47:345-357. https://doi.org/10.1016/S0168-6496(03)00298-8 DOI: https://doi.org/10.1016/S0168-6496(03)00298-8
Grossart HP, Simon M. 2007. Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics. Aquat Microb Ecol. 47:163-176. DOI: https://doi.org/10.3354/ame047163
Guillard RRL. 1973. Division rates. In: Stein JT (ed.), Handbook of phycological methods. Cambridge (UK): Cambridge University Press. p. 289-312.
Hallegraeff GM. 1993. Review of harmful algal blooms and their apparent global increase. Phycology. 32:79-99. https://doi.org/10.2216/i0031-8884-32-2-79.1 DOI: https://doi.org/10.2216/i0031-8884-32-2-79.1
Hallegraeff GM, Blackburn SI, Doblin MA, Bolch CJS. 2011. Global toxicology, ecophysiology and population relationships of the chain forming PST dinoflagellate Gymnodinium catenatum. Harmful Algae. 14:130-143. https://doi.org/10.1016/j.hal.2011.10.018 DOI: https://doi.org/10.1016/j.hal.2011.10.018
Hallegraeff GM, Nichols P, Volkman JK, Blackburn SI, Everitt DA. 1991. Pigments, fatty acids and sterols of the toxic dinoflagellate Gymnodinium catenat J um. Phycol. 27(5):591-599. https://doi.org/10.1111/j.0022-3646.1991.00591.x DOI: https://doi.org/10.1111/j.0022-3646.1991.00591.x
Hernández-Sandoval F, Bustillos-Guzmán JJ, Band-Schmidt CJ, Núñez-Vázquez EJ, López-Cortés DJ, Fernández-Herrera LJ, Poot-Delgado CA, Moreno-Legorreta M. 2022. Effects of different N:P ratios on the growth, toxicity, and toxin profile of Gymnodinium catenatum (Dinophyceae) strains from the Gulf of California. Toxins. 14:501. https://doi.org/10.3390/toxins14070501 DOI: https://doi.org/10.3390/toxins14070501
Hernández-Sandoval FE, López-Cortés DJ, Band-Schmidt CJ, Gárate-Lizárraga I, Núñez-Vázquez EJ, Bustillos-Guzmán JJ. 2009. Toxinas paralizantes en moluscos bivalvos durante una proliferación de Gymnodinium catenatum Graham en la Bahía de La Paz, México. Hidrobiológica. 19:245-256.
Hold GL, Smith EA, Birkbeck TH, Gallacher S. 2001. Comparison of paralytic shellfish toxin (PST) production by the dinoflagellates Alexandrium lusitanicum NEPCC 253 and Alexandrium tamarense NEPCC 407 in the presence and absence of bacteria. FEMS Microbiol Ecol. 36:223-234. https://doi.org/10.1111/j.1574-6941.2001.tb00843.x DOI: https://doi.org/10.1111/j.1574-6941.2001.tb00843.x
Hummert C, Ritscher M, Reinhardt K, Luckas B. 1997. Analysis of the characteristic PSP profiles of Pyrodinium bahamense and several strains of Alexandrium by HPLC based on ion-pair chromatographic separation, post-column oxidation, and fluorescence detection. Chromatographia. 45:312-316. https://doi.org/10.1007/BF02505576 DOI: https://doi.org/10.1007/BF02505576
Jauzein C, Evans AN, Erdner DL. 2015. The impact of associated bacteria on morphology and physiology of the dinoflagellate Alexandrium tamarense. Harmful Algae. 50:65-75. DOI: https://doi.org/10.1016/j.hal.2015.10.006
Kepner RL, Pratt JR. 1994. Use of fluorochromes for direct enumeration of total bacteria in environmental samples: past and present. Aquat Microb Ecol. 54:603-615. https://doi.org/10.1128/mr.58.4.603-615.1994 DOI: https://doi.org/10.1128/MMBR.58.4.603-615.1994
Kirchman D, Sigda J, Kapuscinski R, Mitchell R. 1982. Statistical analysis of the direct count method for enumerating bacteria. Appl Env Microb. 44:376-382. DOI: https://doi.org/10.1128/aem.44.2.376-382.1982
Lin Z-R, Geng H-X, Zhang Q-C, Chen Z-F, Dai L, Yu R-C. 2022. Toxin production of dinoflagellate Gymnodinium catenatum isolated from the East China Sea. Harmful Algae. 113:102188. https://doi.org/10.1016/j.hal.2022.102188 DOI: https://doi.org/10.1016/j.hal.2022.102188
MacKenzie LA. 2014. The risk to New Zealand shellfish aquaculture from paralytic shellfish poisoning (PSP) toxins. N Z J Mar Freshw Res. 48:430-465. https://doi.org/10.1080/00288330.2014.911191 DOI: https://doi.org/10.1080/00288330.2014.911191
Matsumoto M. 2011. Aspects of the interaction between the marine bacterium Alcanivorax DG881 and the toxic dinoflagellate Gymnodinium catenatum [dissertation]. [Australia]: University of Tasmania. 96 p.
Mayali X, Azam F. 2004. Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol. 51:139-144. DOI: https://doi.org/10.1111/j.1550-7408.2004.tb00538.x
Medina-Elizalde J, García-Mendoza E, Turner AD, Sánchez-Bravo YA, Murillo-Martínez R. 2018. Transformation and depuration of paralytic shellfish toxins in the geoduck clam Panopea globosa from the Northern Gulf of California. Front Mar Sci. 5:335. https://doi.org/10.3389/fmars.2018.00335 DOI: https://doi.org/10.3389/fmars.2018.00335
Montoura RFC, Repeta D. 1997. Calibration methods for HPLC. In: SW Jeffrey, Mantoura RFC, Wright SW (eds.), Phytoplankton pigments in oceanography: guidelines to modern methods. Paris (France): UNESCO. p. 407-428.
Moran MA, Miller WL. 2007. Resourceful heterotrophs make the most of light in the coastal ocean. Nat Rev Microbiol. 5:792-800. https://doi:10.1038/nrmi-cro1746. DOI: https://doi.org/10.1038/nrmicro1746
Negri AP, Bolch CJS, Geier S, Green DH, Park T-G, Blackburn SI. 2007. Widespread presence of hydrophobic paralytic shellfish toxins in Gymnodinium catenatum. Harmful Algae. 6:774-780. DOI: https://doi.org/10.1016/j.hal.2007.04.001
Noman MA, Sun J, Gang Q, Guo C, Islam MS, Li S, Yue J. 2019. Factors regulating the phytoplankton and tintinnid microzooplankton communities in the East China Sea. Cont Shelf Res. 181:14-24. https://doi.org/10.1016/j.csr.2019.05.007 DOI: https://doi.org/10.1016/j.csr.2019.05.007
Palomares-García R, Bustillos-Guzmán J, Band-Schmidt CJ, López-Cortés D, Luckas B. 2006. Efecto del dinoflagelado tóxico Gymnodinium catenatum sobre el consumo, la producción de huevos y la tasa de eclosión del copépodo Acartia clausi. Cienc Mar. 32:111-119. DOI: https://doi.org/10.7773/cm.v32i12.1041
Paul C, Pohnert G. 2011. Interactions of the algicidal bacterium Kordia algicida with diatoms: regulated protease excretion for specific algal lysis. PLoS ONE. 6:e21032. https://doi:10.1371/journal.pone.0021032 DOI: https://doi.org/10.1371/journal.pone.0021032
Rippka R, Waterbury JB, Stanier RY. 1981. Isolation and purification of cyanobacteria: some general principles. In: Starr P, Stol P, Triipper H, Balows A, Sahegel H (eds.), The prokaryotes a handbook on habitats, isolation and identification of bacteria. p. 212-220. DOI: https://doi.org/10.1007/978-3-662-13187-9_8
Rooney-Varga JN, Giewat MW, Savin MC, Sood S, LeGresley M, Martin JL. 2005. Links between phytoplankton and bacterial community dynamics in a coastal marine environment. FEMS Microb Ecol. 49:75-163. https://doi.org/10.1007/s00248-003-1057-0 DOI: https://doi.org/10.1007/s00248-003-1057-0
Seibold A, Wichels A, Schütt C. 2001. Diversity of endocytic bacteria in the dinoflagellate Noctiluca scintillans. Aquat Microb Ecol. 25:229-235. DOI: https://doi.org/10.3354/ame025229
Sherr EB, Caron DA, Sherr BF. 1993. Staining of heterotrophic protists for visualization via epifluorescence microscopy. 213-228. In: Kemp P, Sherr B, Sherr E, Cole J (eds.), Current Methods in Aquatic Microbial Ecology. New York (NY): Lewis Publishing Company. DOI: https://doi.org/10.1201/9780203752746-27
Skovgaard A. 2000. A phagotrophically derivable growth factor in the plastidic dinoflagellate Gyrodinium resplendens (Dinophyceae). J Phycol. 36:1096-1078. DOI: https://doi.org/10.1046/j.1529-8817.2000.00009.x
Throndsen J. 1979. Special methods-micromanipulators. In: Stein RJ (ed), Handbook of Phycological Methods: Culture Methods and Growth Measurements. Cambridge (UK): Cambridge University Press. p. 139-144.
Vale P. 2015. Effects of light and salinity stresses in production of mycosporine-like amino acids by Gymnodinium catenatum (Dinophyceae). Photochem Photobiol. 91:1112-1122. DOI: https://doi.org/10.1111/php.12488
Vale P. 2017. Influence of static magnetic fields in phototaxis and osmotic stress in Gymnodinium catenatum (Dinophyceae). Gen Physiol Biophys. 36:235-245. DOI: https://doi.org/10.4149/gpb_2016052
Vidussi F, Claustre H, Bustillos-Guzmán JJ, Cailleau C, Marty JC. 1996. Rapid HPLC method for determination of phytoplankton chemotaxonomic pigments: separation of chlorophyll a from divinyl-chlorophyll a and zeaxanthin from lutein. J Plank Res. 18:2377-2382. DOI: https://doi.org/10.1093/plankt/18.12.2377
Vives CR, Schallenberg C, Strutton PG, Westwood KJ. 2022. Iron and light limitation of phytoplankton growth off East Antarctica. J Mar Syst. 234:103774. https://doi.org/10.1016/j.jmarsys.2022.103774 DOI: https://doi.org/10.1016/j.jmarsys.2022.103774
Wang H, Tomasch J, Jarek M, Wagner-Döbler I. 2014. A dual-species co-cultivation system to study the interactions between Roseobacters and dinoflagellates. Front Microbiol. 5:00311. https://doi.org/10.3389/fmicb.2014.00311 DOI: https://doi.org/10.3389/fmicb.2014.00311
Yu RC, Hummert C, Luckas B, Qian PY, Zhou MJ. 1998. Modified HPLC method for analysis of PSP toxins in algae and shellfish from China. Chromatographia. 48:671-676. https://doi.org/10.1007/BF02467597 DOI: https://doi.org/10.1007/BF02467597
Zar JH. 1999. Biostatistical analysis (4th ed.). Saddle River (NJ): Prentice-Hal. p. 1046. Zheng L, Lin H, Balaji-Prasath B, Su Y, Wang Y, Zheng Y, Yu G. 2023. A novel algicidal properties of fermentation products from Pseudomonas sp. Ps3 strain on the toxic red tide dinoflagellate species. Front Microbiol. 14:1146325. https://doi.org/10.3389/fmicb.2023.1146325 DOI: https://doi.org/10.3389/fmicb.2023.1146325