Cyanobacterium Raphidiopsis raciborskii and its toxin in Buon Phong reservoir, Dak Lak province, Vietnam
Author affiliations
DOI:
https://doi.org/10.15625/2615-9783/16997Keywords:
toxic cyanobacteria, cylindrospermopsin, Buon Phong reservoir, Dak Lak province, VietnamAbstract
This study investigated the variation of the cyanobacterium Raphidiopsis raciborskii population under the influence of physicochemical parameters from May 2019 to April 2020 in the Buon Phong reservoir. The correlations between these parameters were explored by using Principal Component Analysis (PCA) and Pearson correlation analysis. The cylindrospermopsin (CYN) toxin in isolated strains from the reservoir was confirmed by using High-performance liquid chromatography (HPLC) analyses. R. raciborskii presented throughout the year in the reservoir with a biovolume from 0.12 to 9.14 mm3 L-1. Four R. raciborskii strains (CBP2, CBP3, CBP4, and CBP5) were successfully isolated and confirmed to produce CYN by the HPLC results. The highest concentration in isolated strains was 0.345 μg g-1 DW in the CBP4 strain. The PCR results of genes responsible for CYN biosynthesis showed that the PCR amplicons of cyrB and CyrC were amplified in two toxic strains (CBP2 and CBP3), while the amplicons of both cyrB and cyrC were not observed in two remaining toxic strains. In addition, such abiotic factors as temperature and nutrients played major roles in the abundance of R. raciborskii. Moreover, the biovolume of R. raciborskii positively correlated with the CYN concentrations in the Buon Phong reservoir.
Downloads
References
Amaral V., Bonilla S., Aubriot L., 2014. Growth optimization of the invasive cyanobacterium Cylindrospermopsis raciborskii in response to phos-phate fluctuations. Eur J. Phycol., 49, 134-41.
Antunes J.T., Leão P.N., Vasconcelos V.M., 2015. Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species. Front. Microbiol, 6, 1-13.
Babanazarova O.V., Sidelev S.I., Fastner J., 2015. Northern expansion of Cylindrospermopsis raciborskii (Nostocales, Cyanoprokaryota) observed in shallow highly eutrophic lake Nero (Russia). Int. J. Algae, 17, 131-141.
Bai F., Liu R., Yang Y., 2014. Dissolved organic phosphorus use by the invasive freshwater diazotroph cyanobacterium, Cylindrospermopsis raciborskii. Harmful Algae, 39, 112-20.
Barros M.U., Wilson A.E., Leitão J.I., Pereira S.P., Buley R.P., Fernandez-Figueroa, E.G., Capelo-Neto, J., 2019. Environmental factors associated with toxic cyano-bacterial blooms across 20 drinking water reservoirs in a semi-arid region of Brazil. Harmful Algae, 86, 128-137.
Berger C.B.N., Muriel G., Marc B., Filippo R., Alain C., Marc T., Ce ́cile B., 2006. Seaso-nal dynamics and toxicity of Cylindrospermopsis raciborskii in Lake Guiers (Senegal, West Africa). FEMS Microbiol Ecol, 57, 355-366.
Bernard C., Harvey M., Briand J.F., Biré R., Krys S., Fontaine J.J., 2003. Toxicological comparison of diverse Cylindrospermopsis raciborskii strains: evidence of liver damage caused by a French C. raciborskii strain. Environ. Toxicol, 18, 176-186.
Bolius S., Wiedner C., Weithoff G., 2017. High local trait variability in a globally invasive cyanobacterium. Freshwater Biology, 62, 1879-1890.
Bonilla S., Aubriot L., Soares M.C.S., González-Piana M., Fabre A., Huszar V.L.M., Lürling M., Antoniades D., Padisák J., Kruk C., 2012. What drives the distribution of the bloom-forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii? FEMS Microbiology Ecology, 79, 594-607.
Briand J.F., Leboulanger C., Humbert J.F., Bernard C., Dufour P., 2004. Cylindrospermopsis raciborskii (cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming. J Phycol, 40, 231-238.
Burford M.A., Beardall J., Willis A., Orr P.T., Magalhaes V.F., Rangel L.M., Neilan B., 2016. Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae, 54, 44-53.
Burford M.A., Carey C.C., Hamilton D.P., Huisman J., Paerl H.W., Wood S.A., Wulff A., 2020. Perspective: Advancing the research agenda for improving under-standing of cyanobacteria in a future of global change. Harmful Algae, 91, 101601.
Burford M.A., McNeale K.L., McKenzie-Smith F.J., 2006. The role of nitrogen in promoting the toxic cyanophyte Cylindrospermopsis raciborskii in a subtropical water reservoir. Freshwater Biol., 51, 2143-53.
Burford M.A., Willis A., Chuang A., Man X., Orr P., 2018. Recent insights into physiological responses to nutrients by the cylindrospermopsin producing cyanobacterium Cylindrospermopsis raciborskii. Chinese Journal of Oceanology and Limnology, 36, 1032-1039.
Chorus I., eds., 2021. Toxic Cyanobacteria in Water, 2nd edition. CRC Press, Boca Raton (FL), on behalf of the World Health Organization, Geneva, CH, 859pp.
Dao T.S., Cronberg G., Nimptsch J., Do-Hong L.C., Wiegand C., 2010. Toxic cyano-bacteria from Tri An Reservoir, Vietnam. Nova Hedwigia., 90,
-448.
Doyle J.J, Doyle J.L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin, 19, 11-15.
Duong D.T., 1996. Taxonomy of Cyanobacteria of Vietnam. Hanoi: Agriculture Publishing House (in Vietnamese), 189pp.
Duong T.T., Le T.P.Q., Dao T.S., Pflugmacher T., Rochelle-Newall E., Hoang T.K., Vu T.N., Ho TC., Dang D.K., 2013. Seasonal variation of cyanobacteria and microcystins in the Nui Coc Reservoir, Northern Vietnam. Journal of Applied Phycology, 25, 1065-1075.
Everson S., Fabbro L., Kinnear S., Wright P., 2011. Extreme differences in akinete, heterocyte and cylindrospermopsin concentrations with depth in a successive bloom involving Aphanizomenon ovalisporum (Forti) and Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju. Harmful Algae, 10, 265-276.
Fabre A., Carballo C., Hernández E., Piriz P., Bergamino L., Mello L., González S., Pérez G., León J.G., Aubriot L., Bonilla S., Kruk C., 2010. El nitrógeno y la relación zona eufótica/zona de mezcla explican la presencia de cianobacterias en pequeños lagos subtropicales, artificiales de Uruguay. PanAmerican Journal of Aquatic Sciences, 5, 112-125.
Falfushynska H., Horyn O., Brygider A., Fedoruk O., Buyak B., Poznansky D., Poniedziałek B., Kokociński M., Rzymski P., 2018. Is the presence of Central European strains of Raphidiopsis (Cylindrospermopsis) raciborskii a threat to a freshwater fish? An in vitro toxicological study in common carp cells. Aquatic Toxicology, 30901-9.
Fergusson K.M., Saint C.P., 2003. Multiplex PCR assay for Cylindrospermopsis raciborskii and cylindrospermopsin-producing cyanobacteria. Environ Toxicol, 18, 120-125.
Fu L.Q., Yeung C.Y., Fujii M., Neilan B.A., T. David, Waite T.D., 2019. Physiological responses of the freshwater N2-fixing cyanobacterium Raphidiopsis raciborskii to Fe and N availabilities. Environmental Microbiology, 21, 1211-1223.
Galvanese L.F., André A.P., Luis A., 2019. Acclimation at high temperatures increases the ability of Raphidiopsis raciborskii (Cyanobacteria) to withstand phosphate deficiency and reveals distinct strain responses. Journal of Phycology, 54, 359-368.
Hoff-Risseti C., Dörr F.A., Schaker P.D., Pinto E., Werner V.R., Fiore M.F., 2013. Cylindrospermopsin and saxitoxin synthetase genes in Cylindrospermopsis raciborskii strains from Brazilian freshwater. PLoS One, 8, e74238.
Jiang Y., Xiao P., Yu G., Shao J., Liu D., Azevedo S.M.F.O., Li R., 2014. Sporadic distribution and distinctive variations of cylindrospermopsin genes in cyano-bacterial strains and environmental samples from Chinese freshwater bodies. Appl. Environ. Microbiol., 80, 5219-5230.
Karlson B., Cusack C., Bresnan E., 2010. Microscopic and molecular methods for quantitative phytoplankton analysis (IOC Manuals and Guides, no. 55) (IOC/2010/MG/55). UNESCO, Paris.
Kenesi G., Shafik H.M., Kovács A.W., Herodek S., Présing M., 2009. Effect of nitrogen forms on growth, cell composition and N2 fixation of Cylindrospermopsis raciborskii in phosphorus-limited chemostat cultures. Hydrobiologica, 623, 191-202.
Kokocinski M., Jasser I., Karosiene J., Kasperoviciene J., Kobos J., Koreiviene J., Soi-ninen J., Szczurowska A., Woszczyk M., 2017. Distribution of invasive Cylindrospermopsis raciborskii in the East-Central Europe is driven by climatic and local environmental variables. FEMS Microbiol. Ecol., 93, 127-137.
Kokocinski M., Soininen J., 2012. Environmental factors related to the occurrence of Cylindrospermopsis raciborskii (Nostocales, Cyanophyta) at the north-eastern limit of its geographical range. Eur. J. Phycol, 47, 12-21.
Komárek J., Anagnostidis K., 1989. Modern approach to the classification system of cyano-phytes 4- Nostocales. Archiv für Hydrobiologie/Supplements, 56, 247-345.
Komárková J., Laudares-Silva R., Senna P.A.C., 1999. Extreme morphology of Cylindro-spermopsis raciborskii (Nostocales, Cyanobacteria) in the Lagoa do Peri, a freshwater coastal lagoon, Santa Catarina, Brazil. Algol. Stud., 94, 207-222.
Kotai J., 1972. Instructions for preparation of modified nutrient solution Z8 for algae Publication B-11/69. Norwegian Institute for Water Research, Blindern. Oslo 3 Norway.
Le Thuong, 2010. Variation in species composition and number of phytoplankton in EaNhai and EaSup reservoirs, Dak Lak province. PhD thesis in Biology. Vietnam Institute of Science and Technology, Institute of Oceanography, 147pp.
Lei L., Peng L., Xianghui H., Bo-Ping H., 2014. Occurrence and dominance of Cylindrospermopsis raciborskii and dissolved cylindrospermopsin in urban reservoirs used for drinking water supply, South China. Environ Monit Assess., 186, 3079-3090.
Li X., Shouliang H., Jingtian Z., Xiao Z., Beidou X., Renhui L., 2020. Factors related to aggravated Cylindrospermopsis (cyanobacteria) bloom following sediment dredging in an eutrophic shallow lake. Environmental Science and Ecotechnology, 2, 100014.
Lorenzi A.C., Chia M.A., Piccin-Santos V., 2015. Microcystins and cylindrospermopsins molecular markers for the detection of toxic cyanobacteria: a case study of northeastern Brazilian reservoirs. Limnetica, 34, 269-282.
Marbun Y.R., Yen H.K., Lin T.F., Lin H.L., Michinaka A., 2012. Rapid on-site monitoring of cylindrospermopsin-producers in reservoirs using quantitative PCR. Sustain. Environ. Res., 22, 143-151.
Mehnert G., Leunert F., Cires D., 2010. Competitiveness of invasive and native cyanobacteria from temperate freshwaters under various light and temperature conditions. J. Plankton Res., 32, 1009-21.
Meriluoto J., Codd G.A., 2005. Toxic: Cyanobacterial Monitoring and Cyanotoxin Analysis. Åbo Akademi University Press, Åbo, Finland.
Mohamed Z.A., 2007. First report of toxic Cylindrospermopsis raciborskii and Raphidiopsis mediterranea (Cyanoprokariota) in Egyptian fresh waters. FEMS Microbiol. Ecol., 59, 749-761.
Mohamed Z.A., Al-Shehri A.M., 2013. Assessment of cylindrospermopsin toxin in an arid Saudi lake containing dense cyanobacterial bloom. Environ. Monit. Assess., 185, 2157-2166.
Mohamed Z.A., Bakr A., 2018. Concentrations of cylindrospermopsin toxin in water and tilapia fish of tropical fishponds in Egypt, and assessing their potential risk to human health. Environ. Sci. Pollut. Res., 25, 36287-36297.
Ngo T.D.M., Ton T.P., Nguyen T.T.L., 2022. Bloom of harmful cyanobacterium Raphidiopsis raciborskii in Buon Phong reservoir, Dak Lak province. Journal of Science: Natural Science: Hue University, 131, 28-35.
Nguyen T.L., Nguyen T.T.H., Nguyen T.P.T., Pham Q.V., 2021. Assessing trophic status of Suoi Hai Reservoir using Carlson’s Trophic State Index. Vietnam Journal of Earth Sciences, 43, 509-523.
Nguyen T.T.L., Cronberg G., Larsen J., Moestrup Ø., 2007. Planktic cyanobacteria from freshwater localities in Thua Thien-Hue province, Vietnam. I. Morphology and distribution. Nova Hedwigia, 85, 1-34.
Nguyen T.T.L., Hoang T.H., Nguyen T.K., Duong T.T., 2017. The occurrence of toxic cyanobacterium Cylindrospermopsis raciborskii and its toxin cylindrospermopsin in the Huong River, Thua Thien Hue province, Vietnam. Environ Monit Assess., 189, 490.
OECD, 1982. Eutrophication of Waters monitoring, Assessment and Control. Organization for Economic Cooperation and Development, Paris.
Padisák J., 1997. Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: Worldwide distribution and review of its ecology. Archiv Für Hydrobiologie. Supplementband. Monographic Studies, 107, 563-593.
Pagni R.L., Falco P.B., André C.A.S., 2020. Autecology of Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju. Acta Limnologica Brasiliensia, 32, e24.
Pham Q.V., Nguyen T.T.H., Nguyen T.B., Nguyen N.T., La T.O., Nguyen T.P.T., 2019. Developing algorithm for estimating chlorophyll-a concentration in the Thac Ba Reservoir surface water using Landsat 8 Imagery. Vietnam Journal of Earth Sciences, 41, 10-20.
Piccini C., Aubriot L., D’Alessandro B., Martigani F., Bonilla S., 2013. Revealing toxin signatures in cyanobacteria: report of genes involved in cylindrospermopsin synthesis from saxitoxin-producing Cylindrospermopsis raciborskii. Adv. Microbiol, 03, 289-296.
Puerto M., Prieto A.I., Maisanaba S., Gutiérrez-Praena D., Mellado-García P., Jos Á., Cameán A.M., 2018. Mutagenic and genotoxic potential of pure Cylindrospermopsin by a battery of in vitro tests. Food Chem. Toxicol, 121, 413-422.
Rasmussen J.P., Giglio S., Monis P.T., Campbell R.J., Saint C.P., 2008. Development and field testing of a real-time PCR assay for cylindrospermopsin-producing cyanobacteria. J. Appl. Microbiol, 104, 1503-1515.
Recknagel F., Zohary T., Rücker J., Orr P.T., Castelo C., Nixdorf B., Max M.M., 2019. Causal relationships of Raphidiopsis (formerly Cylindrospermopsis) dynamics with water temperature and N:P-ratios: A meta-analysis across lakes with different climates based on inferential modelling. Harmful Algae, 84, 222-232.
Rzymski P., Horyn O., Budzyńska A., Jurczak T., Kokociński M., Niedzielski P., Klimaszyk P., Falfushynska H., 2018. A report of Cylindrospermopsis raciborskii and other cyanobacteria in the water reservoirs of power plants in Ukraine. Environ. Sci. Pollut Res., 25,
-15252.
Shaw G.R., McKenzie R.A., Wickramasinghe W.A., Seawright A.A., Eaglesham G.K., Moore M.R., 2004. Comparative toxicity of the cyanobacterial toxin cylindrospermopsin between mice and cattle: human implications. Harmful Algae, 465-467.
Soares M.C.S., Lürling M., Huszar V.L.M., 2013. Growth and temperature-related phenotypic plasticity in the cyanobacterium Cylindrospermopsis raciborskii. Phycological Research, 61, 61-67.
Stefanova Katerina., Mariana R., Blagoy U., Georg G., Maya S., 2020. Pilot search for cylindrospermopsin producers in nine shallow Bulgarian waterbodies reveals nontoxic strains of Raphidiopsis raciborskii, Raphidiopsis mediterranea and Chrysosporum bergii. Biotechnology & biotechnological equipment, 34, 384-394.
Tawong W., Pongcharoen P., Nishimura T., Adachi M., 2019. Molecular characterizations of Thai Raphidiopsis raciborskii (Nostocales, Cyanobacteria) based on 16S rDNA, rbcLX, and cylindrospermopsin synthetase genes. Plankton Benthos Res., 14, 211-223.
Werner V.R., Andréa T., Lisangela M.S., João S.Y., Emanuel B.N., David E.B., Dail H.L., 2020. Morphological, ecological and toxicological aspects of Raphidiopsis raciborskii (Cyanobacteria) in a eutrophic urban subtropical lake in southern Brazil. Iheringia Serie Botanica, 2446-8231.
Wiedner C., Ruecker J., Brueggemann R., Nixdorf B., 2007. Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions. Oecologia, 152, 473-484.
Williams C.D., Aubel M.T., Chapman A.D., D'Aiuto P.E., 2007. Identification of cyanobacterial toxins in Florida's freshwater systems. Lake Reserv. Manage, 2, 144-152.
Willis A., Chuang, A.W., Woodhouse, J.N. 2016. Intraspecific variation in growth, morphology and toxin quotas for the cyanobacterium, Cylindrospermopsis raciborskii. Toxicon, 119, 307-10.
Willis A., Posselt A.J., Burford M.A., 2017. Variations in carbon-to-phosphorus ratios of two Australian strains of Cylindrospermopsis raciborskii. European Journal of Phycology, 52, 303-310.
Willis A., Woodhouse J.N., Ongley S.E., Jex A.R., Burford M.A., Neilan B.A., 2018. Genome variation in nine cooccurring toxic Cylindrospermopsis raciborskii strains. Harmful Algae, 73, 157-166.
Wood S.A., Pochon X., Luttringer-Plu L., Vant B.N., Hamilton D.P., 2014. Recent invader or indicator of environmental change? A phylogenetic and ecological study of Cylindrospermopsis raciborskii in New Zealand. Harmful Algae, 39, 64-74.
Xiao M., Willis A., Burford M. A., 2017. Differences in cyanobacterial strain responses to light and temperature reflect species plasticity. Harmful Algae, 62, 84-93.
Yamamoto Y., Shiah F.K., 2012. Factors relating to the dominance of Cylindrospermopsis raciborskii (Cyanobacteria) in a shallow pond in northern Taiwan. J. Phycol., 48, 984-991.
Yang Y., Gongliang Y., Youxin C., Nannan J., Renhui L., 2020. Four decades of progress in cylindrospermopsin research: The ins and outs of a potent cyanotoxin. Journal of Hazardous Materials, S0304-3894, 326431.
Yilmaz M., Phlips E.J., Szabo N.J., Badylak S., 2008. A comparative study of Florida strains of Cylindrospermopsis and Aphanizomenon for cylindrospermopsin production. Toxicon, 51, 130-139.
Zhang W., Lou I., Ung W.K., Kong Y., Mok K.M., 2014. Analysis of cylindrospermopsin- and microcystin-producing genotypes and cyanotoxin concentrations in the Macau storage reservoir. Hydrobiologia, 741, 51-68.
Downloads
Published
How to Cite
Issue
Section
