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

Microcystins production and antibacterial activity of cyanobacterial strains of Synechocystis, Synechococcus and Romeria isolated from water and coral reef organisms of Brazilian coast

Giuseppe Barboza, Krystyna Gorlach-Lira, Cristiane Sassi, Roberto Sassi



Cyanobacteria are widely distributed in terrestrial, freshwater and marine environments, and over the past decades have been recognized as a powerful source of bioactive compounds. In this study, some cyanobacterial strains were isolated from samples of seawater, brackish water and tissue of reef benthic invertebrates (zoanthid Protopalythoa variabilis, the sponges Cynachrella sp. and Haliclona sp., the coral Siderastrea stellata, and ascidians), collected at the states of Paraíba and Rio Grande do Norte (Northeast of Brazil), during the period between July 2010 and February 2014. After standard isolation methods, the cultivation of the strains was carried out in acclimatized culture chamber (25 °C) under constant aeration, for 15 days at 12-hour photoperiod, using Conway and BG11 media made with filtered seawater. After ethanolic and methanolic extracts, the strains were analysed for the microcystin production by the ELISA technique and for the antibacterial activity against Staphylococcus aureus and Pseudomonas aeruginosa by the agar well diffusion method. The detection of the mcyB gene, one of the genes related to the microcystin synthesis, was done by the Polymerase Chain Reaction (PCR) technique. The majority of the eighteen cyanobacterial strains belonged to Synechococcaceae Family. The genera of Synechocystis, Synechococcus and Romeria were represented by ten, six and two strains, respectively. The production of microcystins was observed in five strains belonging to the genus Synechocystis. The presence of mcyB gene was detected in 12 strains of cyanobacteria: Synechocystis (three strains), Synechococcus (six strains) and Romeria (two strains). Only one strain (Synechocystis aquatilis) showed both the microcystin production and the mcyB gene presence. The antibacterial activity was observed for one strain of Romeria gracilis, one strain of Synechocystis aquatilis and two strains of Synechococcus sp. The ethanolic extracts of R. gracilis strain and two Synechococcus spp. strains inhibited the growth of P. aeruginosa. Among methanolic extracts of cyanobacteria, only one strain of S. aquatilis showed activity against S. aureus, and one R. gracilis strain against P. aeruginosa. Some cyanobacterial strains studied were positive for the microcystin production and antibacterial activity against pathogenic bacteria S. aureus and P. aeuruginosa, and may be further explored for additional biotechnological applications.


Synechococcales; extracts; mcyB; cyanobacteria.


Al-Wathnani, H., Ara, I., Tahmaz, R. R., Al-Dayel, T. H., & Bakir, M. A. (2012). Bioactivity of natural compounds isolated from cyanobacteria and green algae against human pathogenic bacteria and yeast. Journal of Medicinal Plants Research, 6, 3425-3433. doi:10.5897/JMPR11.1746

Bicudo, C. E. M., & Menezes, M. (2006). Gêneros de Algas de águas continentais do Brasil: chave para identificação e descrições. São Carlos: Rima.

Biondi, N., Tredici, M. R., Taton, A., Wilmotte, A., Hodgson, D. A., Losi, D., & Marinelli F. (2008). Cyanobacteria from benthic mats of Antarctic lakes as a source of new bioactivities. Journal of Applied Microbiology, 105, 105-115. doi:10.1111/j.1365-2672.2007.03716.x

Bittencourt-Oliveira, M. C. (2003). Detection of potential microcystin-producing cyanobacteria in Brazilian reservoirs with a mcyB molecular marker. Harmful Algae, 2, 51-60. doi:10.1016/S1568-9883(03)00004-0

Bittencourt-Oliveira, M. C., Oliveira, M. C., & Pinto, E. (2011). Diversity of microcystin-producing genotypes in Brazilian strains of Microcystis (Cyanobacteria). Brazilian Journal of Biology, 71, 209-216. doi:10.1590/S1519-69842011000100030

Bortoli, S., & Pinto, E. (2015). Cianotoxinas: características gerais, histórico, legislação e métodos de análises. In M. Pompêo, V. Moschini-Carlos, P. Y. Nishimura, S. C. Silva, & J. C. López-Doval (Eds.), Ecologia de reservatórios e interfaces (pp. 321-339). São Paulo: Instituto de Biociências da Universidade de São Paulo.

Brežná, B., & Piknová, L. (2013). Real-time PCR Methods for Identification of Animal or Plant Species (chapter 18). In D. Rodríguez-Lázaro (Eds.), Real-Time PCR in Food Science: Current Technology and Applications (pp. 255-274). Poole: Caister Academic Press.

Caicedo, N. H., Heyduck-Söller, B., Fischer, U., & Thöming, J. (2011). Bioproduction of antimicrobial compounds by using marine filamentous cyanobacterium cultivation. Journal of Applied Phycology, 23, 811-818. doi:10.1007/s10811-010-9580-0

Cardozo, K. H. M., Guaratini, T., Barros, M. P., Falcão, V. R., Tonon, A. P., Lopes, N. P., … & Pinto, E. (2007). Metabolites from algae with economical impact. Comparative Biochemistry and Physiology Part C, 146, 60-78. doi:10.1016/j.cbpc.2006.05.007

Carmichael, W. W., & Li, R. H. (2006). Cyanobacteria toxins in the Salton Sea. Saline Systems, 2(5), 1-13. doi:10.1186/1746-1448-2-5

Costa, M., Costa-Rodrigues, J., Fernandes, M. H., Barros, P., Vasconcelos, V., & Martins, R. (2012). Marine cyanobacteria compounds with anticancer properties: a review on the implication of apoptosis. Marine Drugs, 10, 2181-2207. doi:10.3390/md10102181

Costa, C. F., Sassi, R., & Gorlach-Lira, K. (2008). Uma abordagem metodológica para o estudo das zooxantelas de corais do Brasil. Boletim do Laboratório de Hidrobiologia, 21, 83-94. Retrived from

Dyble, J., Fahnenstiel, G. L., Litaker, R. W., Millie, D. F., & Tester, P. A. (2008). Microcystin concentrations and genetic diversity of microcystis in the lower great lakes. Environmental Toxicology, 23(4), 507-516. doi:10.1002/tox.20370

Ehrenreich, I. M., Waterbury, J. B., & Webb, E. A. (2005). Distribution and diversity of natural product genes in marine and freshwater cyanobacterial cultures and genomes. Applied and Environmental Microbiology, 71, 7401-7413. doi:10.1128/AEM.71.11.7401-7413.2005

Flombaum, P., Gallegos, L. J., Gordillo, A. R., Rincón, J., Zabal, L. L., Jiao, N., ... & Martiny, A. C. (2013). Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proceedings of the National Academy of Sciences of the USA, 110, 9824-9829. doi:10.1073/pnas.1307701110

Franceschini, I. M., Prado, J. F., & Burliga, A. L. (2010). Diversidade das cianobactérias. In I. M. Franceschini, A. L. Burliga, B. Reviers, J. F. Prado, & S. H. Rézig (Eds.), Algas: Uma abordagem filogenética, taxonômica e ecológica (pp. 74-125). Porto Alegre, Rio Grande do Sul: Artmed.

Frazão, B., Martins, R., & Vasconcelos, V. (2010). Are known cyanotoxins involved in the toxicity of picoplanktonic and filamentous North Atlantic marine cyanobacteria? Marine Drugs, 8, 1908-1919. doi:10.3390/md8061908

Gerwick, W. H., Coates, R. C., Engene, N., Gerwick, L., Grindberg, R. V., Jones, A. C., & Sorrels, C. M. (2008). Giant marine cyanobacteria produce exciting potential pharmaceuticals. Microbe, 6, 277-284. doi:10.1128/microbe.3.277.1

Glas, M. S., Motti, C. A., Negri, A. P., Sato, Y., Froscio, S., Humpage, A. R., … & Bourne, D. G. (2010). Cyanotoxins are not implicated in the etiology of coral black band disease outbreaks on Pelorus Island, Great Barrier Reef. FEMS Microbiology Ecology, 73, 43-54. doi:10.1111/j.1574-6941.2010.00874.x

Golubic, S., Abed, R. M. M., Palińska, K., Pauillac, S., Chinain, M., & Laurent, D. (2010). Marine toxic cyanobacteria: Diversity, environmental responses and hazards. Toxicon, 56, 836-841. doi:10.1016/j.toxicon.2009.07.023

Hirose, E., Hirose, M., & Neilan, B. A. (2006). Localization of simbiontic cyanobacteria in the colonial Ascidian Trididemnum miniatum (Didemnidae, Ascidiaceae). Zoological Science, 23, 435-442. doi:10.1111/j.1574-6941.2010.00874.x.

Hoffman, L. (1999). Marine cyanobacteria in tropical regions: diversity and ecology. European Journal of Phycology, 34, 371-379. doi:10.1080/09670269910001736432

Kumar, M., Tripathi, M. K., Srivastava, A., Nath, G., & Asthana, R. K. (2012). A comparative study of antibacterial activity of brackish and fresh water cyanobacterials strains. Asian Journal of Experimental Biology Sciences, 3, 548-542. Retrived from

Leão, P. N., Ramos, V., Gonçalves, P. B., Viana, F., Lage, O. M., Gerwick, W. H., & Vasconcelos, V. M. (2013). Chemoecological screening reveals high bioactivity in diverse culturable portuguese marine cyanobacteria. Marine Drugs, 11, 1316-1335. doi:10.3390/md11041316

Lins de Barros, M. M., Vieira, R. P., Cardoso, A. M., Monteiro, V. A., Turque, A. S., Silveira, C. B., ... & Martins, O. B. (2009). Archaea, bacteria, and algal plastids associated with the reef-building corals Siderastrea stellata and Mussismilia hispida from Búzios, South Atlantic Ocean, Brazil. Microbial Ecology, 59, 523-532. doi:10.1007/s00248-009-9612-y

Lourenço, S. O. (2006). Cultivo de microalgas marinhas - Princípios e aplicações. São Paulo: Rima.

Mackey, R. M. K., Post, A. F., Mcilvin, M. R., Cutterc, G. A., John, S. H., & Saito, M. A. (2015). Divergent responses of Atlantic coastal and oceanic Synechococcus to iron limitation. Proceedings of the National Academy of Sciences of the USA, 112, 9944-9949. doi:10.1073/pnas.1509448112

Madhumathi, V., Deepa, P., Jeyachandran, S., Manoharan, C., & Vijayakumar, S. (2011). Antimicrobial activity of cyanobacteria isolated from freshwater lake. International Journal of Microbiological Research, 2, 213-216. Retrived from

Magalhães, V. F., Marinho, M. M., Domingos, P., Oliveira, A. C., Costa, S. M., Azevedo, L. O., & Azevedo, S. M. (2003). Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brasil, RJ). Toxicon, 42(3), 289-95. doi:10.1016/S0041-0101(03)00144-2

Martins, R., Fernandez, N., Beiras, R., & Vasconcelos, V. (2007). Toxicity assessment of crude and partially purified extracts of marine Synechocystis and Synechococcus cyanobacterial strains in marine invertebrates. Toxicon, 50, 791-799. doi:10.1016/j.toxicon.2007.06.020

Martins, R., Pereira, P., Welker, M., Fastner, J., & Vasconcelos, V. M. (2005). Toxicity of culturable cyanobacteria strains isolated from the Portuguese coast. Toxicon, 46, 454-464. doi:10.1016/j.toxicon.2005.06.010

Martins, R. F., Ramos, M. F., Herfinda, L., Sousa, J. A., Skarven, K., & Vansconcelos, V. M. (2008). Antimicrobial and cytotoxic assessment of marine cyanobacteria - Synechocystis and Synechococcus. Marine Drugs, 6, 1-11. doi:10.3390/md6010001

Nascimento, S. M., & De Oliveira e Azevedo, S. M. F. (1999). Changes in cellular components in a cyanobacterium (Synechocystis aquatilis f. salina) subjected to different N/P ratios - an ecophysiological study. Environmental Toxicology, 14, 37-44. doi:10.1002/(SICI)1522-7278(199902)14:1<37::AID-TOX7>3.0.CO;2-R

Paerl, H. W., & Paul, V. J. (2011). Climate change: Links to global expansion of harmful cyanobacteria. Water Research, 46, 1349-1363. doi:10.1016/j.watres.2011.08.002

Ramos, D. F., Matthiensen, A., Colvara, W., Votto, A. P. S., Trindade, G. S., Silva, P. E. A., & Yunes, J. S. A. (2015). Antimycobacterial activity and cytotoxicity activity of microcystins. Journal of Venomous Animals and Toxins including Tropical Diseases, 21(9), 1-7. doi:10.1186/s40409-015-0009-8

Rogers, S. O., & Bendich, A. J. (1985). Extraction of DNA from milligram amounts of fresh, herbarium mummified plant tissues. Plant Molecular Biology, 5, 69-76. doi:10.1007/BF00020088

Ross, C., Santiago-Vázquez, L., & Paul, V. (2006). Toxin release in response to oxidative stress and programmed cell death in the cyanobacterium Microcystis aeruginosa. Aquatic Toxicology, 78, 66-73. doi:10.1016/j.aquatox.2006.02.007

Senhorinho, G. N. A., Ross, G. M., & Scott, J. A. (2015). Cyanobacteria and eukaryotic microalgae as potential sources of antibiotics. Phycologia, 54, 271-282. doi:10.2216/14-092.1

Singh, R. K., Tiwari, S. P., Rai, A. K., & Mohapatra, T. M. (2011). Cyanobacteria: an emerging source for drug discovery. The Journal of Antibiotics, 64, 401-412. doi:10.1038/ja.2011.21

Siqueira, D. B., & Oliveira-Filho, E. C. (2005). Cianobactérias de água doce e saúde pública: uma revisão. Universitas - Ciências da Saúde, 3, 109-127. doi:10.5102/ucs.v3i1.549

Stanier, R. Y., Kunisawa, R., Mandel, M., & Cohen-Bazire, G. (1971). Purification and properties of unicellular blue green-algae (Order Chroococcales). Bacteriological Reviews, 35, 171-205. Retrived from /articles/PMC378380/

Steindler, L., Huchon, D., Avni, A., & Ilan, M. (2005). 16S rRNA phylogeny of sponge-associated cyanobacteria. Applied and Environmental Microbiology, 71, 4127-4131. doi:10.1128/AEM.71.7.4127-4131.2005

Syiem, M. B., & Bhattacharjee, A. (2010). An efficient protocol for long-term preservation of cyanobacteria. Journal of Advanced Laboratory Research in Biology, 1, 53-59. Retrived from /272635015_an_efficient_protocol_for_long-term_preservation_of _cyanobacteria

Valgas, C., Souza, S. M., Smânia, E. F. A., & Smânia Junior, A. (2007). Screening methods to determine antibacterial activity of natural products. Brazilian Journal of Microbiology, 38, 369-380. doi:10.1590/S1517-83822007000200034

Vareli, K., Zarali, E., Zacharioudakis, G. S. A., Vagenas, G., Varelis, V., Pilidis, G., … & Sainis, I. (2012). Microcystin producing cyanobacterial communities in Amvrakikos Gulf (Mediterranean Sea, NW Greece) and toxin accumulation in mussels (Mytilus galloprovincialis). Harmful Algae, 15, 109-118. doi:10.1016/j.hal.2011.12.005

Volk, R., & Furkert, F. H. (2006). Antialgal, antibacterial and antifungal activity of two metabolites produced and excreted by cyanobacteria during growth. Microbiological Research, 161, 180-186. doi:10.1016/j.micres.2005.08.005

Walne, P. R. (1970). Studies on the food values of nineteen genera of algae to juvenile bivalves of the genera Ostrea, Crassostrea, Mercenaria and Mytilus. Fishery Investigations, Series II, 26, 62. London, UK: H.M.S.O.


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