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Biodiversity and toxin production of cyanobacteria in mangrove swamps in the Red Sea off the southern coast of Saudi Arabia

  • Zakaria A. Mohamed

    Zakaria A. Mohamed obtained his BSc and MSc from Assiut University, Egypt, and completed his PhD at Wright State University, OH, USA. He worked as an Assistant and an Associate Professor in the Botany Department of Assiut University. From 2003 to 2011, he held a position as a Visiting Professor for teaching and research at King Khalid University, Saudi Arabia. Currently, he is a Professor of Phycology/Phycotoxins at the Botany Department, Faculty of Science, Sohag University, Egypt. He has served as a reviewer for various international journals and was an invited speaker at the 1st International Conference on Toxins in Desert Environments, Weill Cornell Medical College, Qatar (2013). His research interests focus on toxin production in freshwater and marine cyanobacteria and microalgae, and the impacts of these toxins on aquatic and terrestrial environments.

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    and Abdulrahman M. Al-Shehri
From the journal Botanica Marina

Abstract

This study investigated the diversity and toxin production of cyanobacteria forming microbial mats on the soil surface and mangrove pneumatophores in three different mangrove swamps in the Red Sea off the southern coast of Saudi Arabia. In total, 34 species belonging to 15 genera and five families were recorded. Benthic mats had higher numbers of species (25–31) than pneumatophore mats (10–12). Cyanobacterial biodiversity (H) and species evenness (E) were greater in benthic mats (H=2.52–2.83 and E=0.79–0.83) than in pneumatophore mats (H=1.7–1.82 and E=0.73–0.74). The results showed high similarity of species between different mangrove sites (67.6%–91.7%) and low similarity between benthic and pneumatophore mats at the same site (32.3%–35.75%). During this study, only nine cyanobacterial species were successfully isolated and tested for their toxicity. The extracts of these species exhibited toxicity to Artemia salina (LC50=0.3–5.1 mg l-1). Based on the results of ELISA and HPLC analyses, four species were found to produce microcystins (683–974 μg g-1) and three species produced saxitoxins (58.9–93.8 μg g-1). The presence of toxic cyanobacteria and their toxins in mangrove swamps may pose a risk for marine animals because these toxins can accumulate in aquatic food webs with a potential for transfer to higher trophic levels.


Corresponding author: Zakaria A. Mohamed, Faculty of Science, Department of Botany, Sohag University, Sohag 82524, Egypt, e-mail:

About the author

Zakaria A. Mohamed

Zakaria A. Mohamed obtained his BSc and MSc from Assiut University, Egypt, and completed his PhD at Wright State University, OH, USA. He worked as an Assistant and an Associate Professor in the Botany Department of Assiut University. From 2003 to 2011, he held a position as a Visiting Professor for teaching and research at King Khalid University, Saudi Arabia. Currently, he is a Professor of Phycology/Phycotoxins at the Botany Department, Faculty of Science, Sohag University, Egypt. He has served as a reviewer for various international journals and was an invited speaker at the 1st International Conference on Toxins in Desert Environments, Weill Cornell Medical College, Qatar (2013). His research interests focus on toxin production in freshwater and marine cyanobacteria and microalgae, and the impacts of these toxins on aquatic and terrestrial environments.

Acknowledgments

The authors would like to thank Dr. Ahmed Al-Qahtani, Research Center, Toxicology and Bioanalysis Section, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia, for LC-MS/MS analysis.

References

Abed, R.M.M., S. Golubic, F. Garcia-Pichel, G. Camoin and S. Sprachta. 2003. Characterization of microbialite-forming cyanobacteria in a tropical lagoon: Tikehau Atoll, Tuamotu, French Polynesia. J. Phycol.39: 862–873.10.1046/j.1529-8817.2003.02180.xSearch in Google Scholar

Abed, R.M.M., S. Dobrestov, S. Al-Kharusi, A. Schramm, B. Jupp and S. Golubic. 2011. Cyanobacterial diversity and bioactivity of inland hypersaline microbial mats from a desert stream in the Sultanate of Oman. Fottea 11: 215–224.10.5507/fot.2011.020Search in Google Scholar

Allen, M.M. 1984. Cyanobacterial cell inclusions. Annu. Rev. Microbiol. 38: 1–2.10.1146/annurev.mi.38.100184.000245Search in Google Scholar

Al-Shehri, A.M. and Z.A. Mohamed. 2007. Mass occurrence and toxicity of the cyanobacterium Lyngbya majuscula under phosphorus-limited conditions in the Red Sea. Ecohydrol. Hydrobiol.7: 51–57.10.1016/S1642-3593(07)70188-XSearch in Google Scholar

Anagnostidis, K. and J. Komárek. 1988. Modern approach to the classification system of cyanophytes. 3. Oscillatoriales. Arch. Hydrobiol. 80/Algol. Stud. 5053: 327–472.Search in Google Scholar

Carmichael, W.W. and R.H. Li. 2006. Cyanobacteria toxins in the Salton Sea. Saline Syst. 2: 1–13.10.1186/1746-1448-2-5Search in Google Scholar PubMed PubMed Central

Dorador, C., I. Vila, J.F. Imhoff and K.-P. Witzel. 2008. Cyanobacterial diversity in Salar de Huasco, a high altitude saline wetland in northern Chile: an example of geographical dispersion?.FEMS Microbiol. Ecol.64: 419–432.Search in Google Scholar

El-Juhany, L.I. 2009. Present status and degradation trends of mangrove forests on the southern Red Sea coast of Saudi Arabia. Am. Euras. J. Agric. Environ. Sci.6: 328–340.Search in Google Scholar

Feller, I.C., C.E. Lovelock, U. Berger, K.L. McKee, S.B. Joye and M.C. Ball. 2010. Biocomplexity in mangrove ecosystems. Annu. Rev. Mar. Sci. 2: 395–417.10.1146/annurev.marine.010908.163809Search in Google Scholar PubMed

Frazão B., R. Martins and V. Vasconcelos. 2010. Are known cyanotoxins involved in the toxicity of picoplanktonic and filamentous North Atlantic marine cyanobacteria? Mar. Drugs8: 1908–1919.10.3390/md8061908Search in Google Scholar PubMed PubMed Central

Gantar, M., R. Sekar and L.L. Richardson. 2009. Cyanotoxins from black band disease of corals and from other coral reef environments. Microb. Ecol.58: 856–864.10.1007/s00248-009-9540-xSearch in Google Scholar PubMed PubMed Central

Garcia-Pichel, F., I. Prufert-Bebout and G. Muyzer. 1996. Phenotypic and phylogenetic analyses show Microcoleus chthonoplastes to be a cosmopolitan cyanobacterium. App.Environ. Microbiol.62: 3284–3291.10.1128/aem.62.9.3284-3291.1996Search in Google Scholar PubMed PubMed Central

Hamisi M.I., T.J. Lyimo and M.H.S. Muruke. 2004. Cyanobacterial occurrence and diversity in seagrass meadows in coastal Tanzania. Western Indian Ocean J. Mar. Sci. 3: 113–122.10.4314/wiojms.v3i2.28455Search in Google Scholar

Hicks, B. and W. Silverster. 1985. Nitrogen fixation associated with New Zealand mangrove (Avicennia marina (Forsk) Vierh. var. resinifera Forrsk. f. Bakl). Appl. Environ. Microbiol. 49: 955–959.10.1128/aem.49.4.955-959.1985Search in Google Scholar

Hindell, J.S. and G.P. Jenkins. 2004. Spatial and temporal variability in the assemblage structure of fishes associated with mangroves (Avicennia marina) and intertidal mudflats in temperate Australian embayments. Mar. Biol. 144: 385–395.10.1007/s00227-003-1201-xSearch in Google Scholar

Hogarth, P.J. 1999. The biology of mangroves. Oxford University Press, New York.Search in Google Scholar

Hong, J.W., H.-G. Choi, S.-H. Kang and H.-S. Yoon. 2010. Axenic purification and cultivation of an arctic cyanobacterium, Nodularia spumigena KNUA005, with cold tolerance potential for sustainable production of algae-based biofuel. Algae 25: 99–104.Search in Google Scholar

Hussain, M.I. and T.M. Khoja. 1993. Intertidal and subtidal blue-green algal mats of open and mangrove areas in the Farasan Archipelago (Saudi Arabia) Red sea. Bot. Mar.36: 377–388.10.1515/botm.1993.36.5.377Search in Google Scholar

Kathiresan, K. and B.L. Bingham. 2001. Biology of mangroves and mangrove ecosystems. Adv. Mar. Biol.40: 81–251.10.1016/S0065-2881(01)40003-4Search in Google Scholar

Komárek, J. and K. Anagnostidis. 1989. Modern approach to the classification system of Cyanophytes. 4. Nostocales. Algol. Stud.82: 247–345.Search in Google Scholar

Komárek, J. and K. Anagnostidis. 2005. Cyanoprokaryota. 2. Teil: Oscillatoriales. In: (B. Büdel, L. Krienitz, G. Gärtner and M. Schagerl, eds) Süsswasserflora von Mitteleuropa. Elsevier GmbH, Munich. pp. 1–759.Search in Google Scholar

Kotai, J. 1972. Instructions for preparation of modified nutrient solution Z8 for algae. Norwegian Institute for Water Research, Blindern, Oslo, Norway.Search in Google Scholar

Kyaruzi, J.J., M.S. Kyewalyanga and M.H.S. Muruke. 2003. Cyanobacteria composition and impact of seasonality on their in situ nitrogen fixation rate in a mangrove ecosystem adjacent to Zanzibar town. Western Indian Ocean J. Mar. Sci.2: 35–44.10.4314/wiojms.v2i1.28427Search in Google Scholar

Lopes, V.R., N. Fernández, R.F. Martins and V. Vasconcelos. 2010. Primary screening of the bioactivity of brackishwater cyanobacteria: toxicity of crude extracts to Artemia salina larvae and Paracentrotus lividus embryos. Mar. Drugs 8: 471–482.10.3390/md8030471Search in Google Scholar

Lopes, V.R., V. Ramos, A. Martins, M. Sousa, M. Welker, A. Antunes and V.M. Vas-concelos. 2012. Phylogenetic, chemical and morphological diversity of cyanobacteria from Portuguese temperate estuaries. Mar. Environ. Res.73: 7–16.Search in Google Scholar

Mani, P. 1992. Natural phytoplankton communities in Pichavaram mangroves. Indian J. Mar. Sci. 21: 278–280.Search in Google Scholar

Martins, R., P. Pereira, M. Welker, J. Fastner and V.M. Vasconcelos. 2005. Toxicity of culturable cyanobacteria strains isolated from the Portuguese coast. Toxicon46:454–464.10.1016/j.toxicon.2005.06.010Search in Google Scholar PubMed

Martins, R., N. Fernandez, R. Beiras and V. Vasconcelos. 2007. Toxicity assessment of crude and partially purified extracts of marine Synechocystis and Synechococcus cyanobacterial strains in marine invertebrates. Toxicon50:791–799.10.1016/j.toxicon.2007.06.020Search in Google Scholar PubMed

Mohamed, Z.A., H.M. El-Sharouny and W.S.M. Ali. 2006. Microcystin production in benthic mats of cyanobacteria in the Nile River and irrigation canals, Egypt. Toxicon 47: 584–590.10.1016/j.toxicon.2006.01.029Search in Google Scholar PubMed

Nagarkar S., G.A. Williams, G. Subramanian and S.K. Saha. 2004. Cyanobacteria-dominated biofilms: a high quality food resource for intertidal grazers. Hydrobiol. 512: 89–95.10.1023/B:HYDR.0000020313.09924.c1Search in Google Scholar

Nagasathya, A. and N. Thajuddin. 2008. Cyanobacterial diversity in the hypersaline environment of the saltpans of south eastern coast of India. Asian J. Plant Sci.7: 473–478.10.3923/ajps.2008.473.478Search in Google Scholar

Nogueira, N.M. and M.M. Ferreira-Correia. 2001. Cyanophyceae/cyanobacteria in red mangrove forest at Mosquitos and Coqueiros estuaries, São Luís, State of Maranhão, Brazil. Braz. J. Biol. 61: 347–356.10.1590/S1519-69842001000300002Search in Google Scholar PubMed

Parsons, T.R., Y. Maita and C.M. Lalli. 1989. A manual of chemical and biological methods for sea water analysis. Pergamon Press, Oxford. pp. 14–17.Search in Google Scholar

Perona, E., I. Bonilla and P. Mateo. 1998. Epilithic cyanobacterial communities and water quality: an alternative tool for monitoring eutrophication in the Alberche River (Spain). J. Appl. Phycol. 10:183–191.10.1023/A:1008051327689Search in Google Scholar

Pyle, B., S.C. Broadaway and G.A. McFeters. 1995. A direct method for enumerating respiring enterohemmorhagic E. coli 0157H7 in water. Appl. Environ. Microbiol. 61: 2514–2519.10.1128/aem.61.7.2614-2619.1995Search in Google Scholar PubMed PubMed Central

Rapala, J., K. Erkomaa, J. Kukkonen, K. Sivonen and K. Lahti. 2002. Detection of microcystins with protein phosphatase inhibition assay, high-performance liquid chromatography-UV-detection and enzyme-linked immunosorbent assay: comparison of methods. Anal. Chim. Acta.466: 213–231.Search in Google Scholar

Richardson, L.L., R. Sekar, J.L. Myers, M. Gantar, J.D. Voss, L. Kaczmarsky, E.R. Remily, G.L. Boyer and P.V. Zimba. 2007. The presence of the cyanobacterial toxin microcystin in black band disease of corals. FEMS Microbiol. Lett.272: 182–187.10.1111/j.1574-6968.2007.00751.xSearch in Google Scholar PubMed

Rigonato, J., D.O. Alvarenga, F.D. Andreote, A.C.F. Dias, I.S. Melo, A. Kent and M.F. Fiore. 2012. Cyanobacterial diversity in the phyllosphere of a mangrove forest. FEMSMicrobiol. Ecol. 80: 312–322.10.1111/j.1574-6941.2012.01299.xSearch in Google Scholar PubMed

Rigonato, J., A.D. Kent, D.O. Alvarenga, F.D. Andreote, R.M. Beirigo, P. Vidal-Torrado and M.F. Fiore. 2013. Drivers of cyanobacterial diversity and community composition in mangrove soils in South-east Brazil. Environ. Microbiol.15: 1103–1114.10.1111/j.1462-2920.2012.02830.xSearch in Google Scholar PubMed

Rippka, R., J. Deruelles, J.B. Waterbury and R.Y. Stanier. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol.111: 1–61.Search in Google Scholar

Sakthivel K. and K. Kathiresan. 2013. Cyanobacterial diversity from mangrove sediment of south east coast of India. Asian J. Biodiversity4: 190–203.10.7828/ajob.v4i1.303Search in Google Scholar

Shannon, C.E. and W. Weaver. 1963. The mathematical theory of communication. University of Illinois Press, Urbana, IL. pp. 125.Search in Google Scholar

Silambarasan, G., T. Ramanathan and K. Kathiresan. 2012. Diversity of marine cyanobacteria from three mangrove environment in Tamil Nadu Coast, south east coast of India. Curr. Res. J. Biol. Sci.4: 235–238.Search in Google Scholar

Silva, C.S.P., D.B. Genuário, M.G. Marc, A.-V. Vaz and M.F. Fiore. 2014. Phylogeny of culturable cyanobacteria from Brazilian mangroves. Syst. Appl. Microbiol.37: 100–112.10.1016/j.syapm.2013.12.003Search in Google Scholar PubMed

Singh, S., B.N. Kate and U.C. Banerjee. 2005. Bioactive compounds from cyanobacteria and microalgae: an overview. Crit. Rev. Biotechnol. 25: 73–95.10.1080/07388550500248498Search in Google Scholar PubMed

Spalding, M., F. Blasco and C. Field. 1997. World mangrove atlas. The International Society for Mangrove Ecosystems, Okinawa, Japan. pp. 178.Search in Google Scholar

Sprachta, S., G. Camoin, S. Golubic and T. Le Campion. 2001. Microbialites in a modern lagoonal environment: nature and distribution, Tikehau atoll (French Polynesia). Palaeogeogr. Palaeoclimatol. Palaeoecol.175: 103–124.Search in Google Scholar

Staal, M., F.J.R. Meysman and L.J. Stal. 2003. Temperature excludes N2-fixing heterocystous cyanobacteria in the tropical oceans. Nature 425: 504–507.10.1038/nature01999Search in Google Scholar PubMed

Stal, L.J. 1995. Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytol.131: 1–32.10.1111/j.1469-8137.1995.tb03051.xSearch in Google Scholar PubMed

Stal, L.J., S.B. Behrens and M. Villbrandt. 1996. The biogeochemistry of two eutrophic marine lagoons and its effect on microphytobenthic communities Hydrobiol. 329: 185–198.10.1007/978-94-009-1744-6_15Search in Google Scholar

Stanić, D., S. Oehrle, M. Gantar and L.L. Richardson. 2011. Microcystin production and ecological physiology of Caribbean black band disease cyanobacteria. Environ. Microbiol.14: 900–910.10.1111/j.1462-2920.2010.02388.xSearch in Google Scholar PubMed

Sugumar, R., G. Ramanathan, K. Rajarathinam, A. Jeevarathinam, D. Abirami and M. Bhoothapandi. 2011. Diversity of saltpan marine cyanobacteria from Cape Comorin coast of Tamilnadu. J. Phytol. 3: 1–4.Search in Google Scholar

Sundararaman, M., T. Boopathi and S. Gopinath. 2007. Status of mangrove ecosystem: exploring the potential role of cyanobacteria in restoration and afforestation. In: (S. Joseph, ed) Algae and cyanobacteria in extreme environments. Springer, Netherlands. pp. 211–224.Search in Google Scholar

Thajuddin, N. and G. Subramanian. 2005. Cyanobacterial biodiversity and potential application in biotechnology. Curr. Sci.89: 47–57.Search in Google Scholar

Villeneuve, A., D. Laurent, M. Chinain, M. Gugger and J.F. Humbert. 2012. Molecular characterization of the diversity and potential toxicity of cyanobacterial mats in two tropical lagoons in the South Pacific Ocean. J. Phycol.48: 275–284.10.1111/j.1529-8817.2012.01118.xSearch in Google Scholar PubMed

Watkinson, A.J., J.M. O’Neil and W.C. Dennison. 2005. Ecophysiology of the marine cyanobacterium, Lyngbya majuscula (Oscillatoriaceae) in Moreton Bay, Australia. Harmful Algae4: 697–715.10.1016/j.hal.2004.09.001Search in Google Scholar

Received: 2014-9-11
Accepted: 2015-1-8
Published Online: 2015-1-30
Published in Print: 2015-2-1

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