Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

The inhibitory effect of a non-yessotoxin-producing dinoflagellate, Lingulodinium polyedrum (Stein) Dodge, towards Vibrio vulnificus and Staphylococcus aureus
PT 64-2 JUN 2016

Supplementary Files



Proliferaciones algales
resistencia bacteriana
Lingulodinium polyedrum
Staphylococcus aureus
Vibrio vulnificus

How to Cite

Quijano-Scheggia, S., Barajas-Gonzalez, M., Chang Lim, H., Pin Leaw, C., Olivos-Ortiz, A., Gaviño-Rodriguez, J., Blanco Pérez, J., & Bates, S. S. (2016). The inhibitory effect of a non-yessotoxin-producing dinoflagellate, Lingulodinium polyedrum (Stein) Dodge, towards Vibrio vulnificus and Staphylococcus aureus. Revista De Biología Tropical, 64(2), 805–816.


The increased bacterial resistance to antibiotics has caused global concern, prompting the search for new compounds. Because of their abundance and diversity, marine phytoplankton is an important potential source of such compounds. Research on dinoflagellates has led to the discovery of inhibitors of bacterial growth. The marine dinoflagellate Lingulodinium polyedrum blooms in different regions of the world, including Mexico, and is also known to regulate the growth of other species in coastal waters. Here, we investigated the taxonomy of this dinoflagellate and characterized the ability of its extracts to inhibit the growth of two bacteria of medical importance (Vibrio vulnificus and Staphylococcus aureus). Taxonomic characterization was performed by PCR and gene amplification of ITS, and confirmed that the species isolated off the Pacific coast of Mexico was L. polyedrum. To prove the inhibitory effect of L. polyedrum extracts, cultures were harvested by centrifugation. Pellets from three cellular abundances were extracted with water, methanol, hexane and chloroform. The experiments on V. vulnificus showed a high growth inhibition for the four extracts, ranging from 77 to 98 %. Surprisingly, the growth inhibition was lower when the extracts originated from a higher L. polyedrum cell abundance, ranging from 0 to 34 %. For S. aureus, the growth inhibition was also high, but not statistically different for all extracts and cell abundances, ranging from 62 to 99 %. This study obtained promising results for future pharmacological applications. Our Mexican strain of L. polyedrum did not produce any detectable yessotoxins.


Anderson, R. A. (1996). Algae. In J. C. Hunter-Cevera, & A. Belt (Eds.), Maintaining cultures for biotechnology and industry (pp. 29-64). San Diego: Academic Press.

Appelbaum, P. C. (2007). Microbiology of antibiotic resistance in Staphylococcus aureus. Clinical Infectious Diseases, 45(3), 165-170.

Armstrong, M., & Kudela, R. (2006). Evaluation of California isolates of Lingulodinium polyedrum for the production of yessotoxin. African Journal of Marine Science, 28(5), 399-401.

Band-Schmidt, C. J., Bustillos-Guzmán, J., Gárate-Lizárraga, I., Lechuga-Devéze, C. H., 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, México. Harmful Algae, 4(1), 21-31.

Blunt, J. W., Copp, B. R., Munro, M. H. G., Northcote, P. T., & Prinsep, M. R. (2011). Marine natural products. Natural Product Reports, 28(2), 196-268.

Camacho, F. G., Rodríguez, J. G., Mirón, A. S., García, M. C., Belarbi, E., Chisti, Y., & Grima, E. M. (2007). Biotechnological significance of toxic marine dinoflagellates. Biotechnology Advances, 25(2), 176-194.

Darty, K., Denise, A., & Ponty, Y. (2009). VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics, 25(15), 1974-1975.

de Jesus Raposo, M. F., de Morais, R. M. S. C., & de Morais, A. M. M. B. (2013). Health applications of bioactive compounds from marine microalgae. Life Sciences, 93(15), 479-486.

del Pilar Sánchez-Saavedra, M., Licea-Navarro, A., & Bernáldez-Sarabia, J. (2010). Evaluation of the antibacterial activity of different species of phytoplankton. Revista de Biología Marina y Oceanografía, 45(3), 531-536.

Desbois, A. P., Mearns-Spragg, A., & Smith, V. J. (2009). A fatty acid from the diatom Phaeodactylum tricornutum is antibacterial against diverse bacteria including multi-resistant Staphylococcus aureus (MRSA). Marine Biotechnology, 11(1), 45-52.

Fischbach, M. A., & Walsh, C. T. (2009). Antibiotics for emerging pathogens. Science, 325 (5944), 1089-1093.

Gallardo-Rodríguez, J., Sánchez-Mirón, A., García-Camacho, F., López-Rosales, L., Chisti, Y., & Molina-Grima, E. (2012). Bioactives from microalgal dinoflagellates. Biotechnology Advances, 30(6), 1673-1684.

Garrido, R., Lagos, N., Lattes, K., Abedrapo, M., Bocic, G., Cuneo, A., Chiong, H., Jensen, C., Azolas, R., & Henriquez, A. (2005). Gonyautoxin: new treatment for healing acute and chronic anal fissures. Diseases of the Colon & Rectum, 48, 335-343.

Guillard, R. R. L. (1975). Culture of phytoplankton for feeding marine invertebrates In W. L. Smith, & M. H. Chanley (Eds.), Culture of marine invertebrate animals (pp. 29-60). New York: Plenum Publ. Corp.

Horseman, M. A., & Surani, S. (2011). A comprehensive review of Vibrio vulnificus: an important cause of severe sepsis and skin and soft-tissue infection. International Journal of Infectious Diseases, 15(3), 157-166.

Kim, J. H., Choresca, C. H. Jr., Shin, S. P., Han, J. E., Jun, J. W., & Park, S. C. (2011). Occurrence and antibiotic resistance of Vibrio vulnificus in seafood and environmental waters in Korea. Journal of Food Safety, 31(4), 518-524.

Klevens, R. M., Morrison, M. A., Nadle, J., Petit, S., Gershman, K., Ray, S., Harrison, L. H., Lynfield, R., Dumyati, G., & Townes, J. M. (2007). Invasive methicillin-resistant Staphylococcus aureus infections in the United States. Journal of the American Medical Association, 298(15), 1763-1771.

Koetschan, C., Förster, F., Keller, A., Schleicher, T., Ruderisch, B., Schwarz, R., Müller, T., Wolf, M., & Schultz, J. (2010). The ITS2 Database III—sequences and structures for phylogeny. Nucleic Acids Research, 38(1), D275-D279.

Kofoid, C. A. (1911). Dinoflagellata of the San Diego region. IV. The genus Gonyaulax, with notes on its skeletal morphology and a discussion of its generic and specific characters. University of California Publications in Zoology, 8(4-6), 187-286.

Konishi, M., Yang, X., Li, B., Fairchild, C. R., & Shimizu, Y. (2004). Highly cytotoxic metabolites from the culture supernatant of the temperate dinoflagellate Protoceratium cf. reticulatum. Journal of Natural Products, 67(8), 1309-1313.

Kumar, S., Tamura, K., & Nei, M. (2004). MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics, 5(2), 150-163.

Lowy, F. D. (2003). Antimicrobial resistance: the example of Staphylococcus aureus. Journal of Clinical Investigation, 111(9), 1265-1273.

Lundholm, N., Moestrup, Ø., Hasle, G. R., & Hoef-Emden, K. (2003). A study of the Pseudo-nitzschia pseudodelicatissima/cuspidata complex (Bacillariophyceae): What is P. pseudodelicatissima? Journal of Phycology, 39, 797-813.

Mai, J. C., & Coleman, A. W. (1997). The internal transcriber spacer 2 exhibits a common secondary structure in green algae and flowering plants. Journal of Molecular Evolution, 44(3), 258-271.

Mathews, D. H., Disney, M. D., Childs, J. L., Schroeder, S. J., Zuker, M., & Turner, D. H. (2004). Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proceedings of the National Academy of Sciences of the United States America, 101(19), 7287-7292.

Morquecho, L., & Lechuga-Devéze, C. H. (2004). Seasonal occurrence of planktonic dinoflagellates and cyst production in relationship to environmental variables in subtropical Bahía Concepción, Gulf of California. Botanica Marina, 47, 313-322.

Paul, J. H. (2011). Amplifying the target nucleotide sequence of the polyketide synthetase gene to produce an amplified polynucleotide; detecting the presence of the amplified polynucleotide by contacting the amplified polynucleotide with a labeled molecular beacon; for determining the virulence of red tide blooms. Google Patents.

Paz, B., Riobó, P., Fernández, M. L., Fraga, S., & Franco, J. M. (2004). Production and release of yessotoxins by the dinoflagellates Protoceratium reticulatum and Lingulodinium polyedrum in culture. Toxicon, 44(3), 251-258.

Paz, B., Daranas, A. H., Norte, M., Riobó, P., Franco, J. M., & Fernández, J. J. (2008). Yessotoxins, a group of marine polyether toxins: an overview. Marine Drugs, 6(2), 73-102.

Peña-Manjarrez, J. L., Gaxiola-Castro, G., & Helenes-Escamilla, J. (2009). Environmental factors influencing the variability of Lingulodinium polyedrum and Scrippsiella trochoidea (Dinophyceae) cyst production. Ciencias Marinas, 35(1), 1-14.

Pérez-Morales, A., Band-Schmidt, C. J., Ortíz-Galindo, J. L., & Sobrino-Figueroa, A. S. (2014). Mortality in the initial ontogeny of Paralabrax maculatofasciatus (Actinopterygii, Perciformes, Serranidae) caused by Chattonella spp. (Raphidophyceae). Hydrobiologia, 722(1), 247-261.

Regueiro, J., Martín-Morales, E., Álvarez, G., & Blanco, J. (2011). Sensitive determination of domoic acid in shellfish by on-line coupling of weak anion exchange solid-phase extraction and liquid chromatography–diode array detection–tandem mass spectrometry. Food Chemistry, 129(2), 672-678.

Quijano-Scheggia, S., Olivos-Ortiz, A., Rivera-Vilarelle, M., Gaviño-Rodríguez, J., Álvarez, C., & Sosa-Avalos, R. (2013). Cuatro años de monitoreo de fitoplancton en las Bahías de Manzanillo y Santiago. Segundo congreso Somefan. Universidad de Colima, Mazanillo, Colima.

Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12), 1572-1574.

Ruiz-de la Torre, M. C., Maske, H., Ochoa, J., & Almeda-Jauregui, C. O. (2013). Maintenance of coastal surface blooms by surface temperature stratification and wind drift. PLoS One, 8(4), e58958.

Schultz, J., Müller, T., Achtziger, M., Seibel, P. N., Dandekar, T., & Wolf, M. (2006). The internal transcribed spacer 2 database—a web server for (not only) low level phylogenetic analyses. Nucleic Acids Research, 34, W704-W707.

Selander, E., & Pavia, H. (2008). Method to enhance production of paralytic shellfish toxins from dinoflagellate cultures. Google Patents.

Selig, C., Wolf, M., Müller, T., Dandekar, T., & Schultz, J. (2008). The ITS2 Database II: homology modelling RNA structure for molecular systematics. Nucleic Acids Research, 36(1), D377-D380.

Shanmugapriya, R., & Ramanathan, T. (2011). Screening for antimicrobial activity of crude extracts of Skeletonema costatum. Journal of Applied Pharmaceutical Science, 1(7), 154-157.

Shaw, K. S., Goldstein, R. E. R., He, X., Jacobs, J. M., Crump, B. C., & Sapkota, A. R. (2014). Antimicrobial susceptibility of Vibrio vulnificus and Vibrio parahaemolyticus recovered from recreational and commercial areas of Chesapeake Bay and Maryland coastal bays. PLoS One, 9(2), e89616.

Smayda, T. J., & Trainer, V. L. (2010). Dinoflagellate blooms in upwelling systems: seeding, variability, and contrasts with diatom bloom behavior. Progress in Oceanography, 85(1-2), 92-107.

Stach, J. (2010). Antimicrobials: treasures from the oceans. Microbiology Today, 37(2), 104-109.

Strom, M. S., & Paranjpye, R. N. (2000). Epidemiology and pathogenesis of Vibrio vulnificus. Microbes and Infection, 2(2), 177-188.

Thompson, J. D., Higgins, D. G., & Gibbson, T. J. (1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22), 4673-4680.

Throndsen, J. (1995). Estimating cell numbers. In G. M. Hallegraeff, D. M. Anderson, & A. D. Cembella (Eds.), Manual on harmful marine microalgae. IOC Manual and Guides (pp. 63-80). Paris: UNESCO.

Tomas, C. R. (1997). Identifying marine phytoplankton. San Diego: Academic Press.

Tortora, G. J., Funke, B. R., & Case C. L. (2007). Introducción a la Microbiología. Buenos Aires. Médica Panamericana.

Utermöhl, H. (1931). Neue Wege in der quantitativen Erfassung des Planktons. Verhandlungen des Internationalen Verein Limnologie, 5, 567-95.

White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: a guide to methods and applications (pp. 315-322). New York: Academic Press.



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