Physical and chemical processes promoting dominance of the toxic cyanobacterium Cylindrospermopsis raciborskii

Chinese Journal of Oceanology and Limnology

Volumn 29, Issue 4, 2011, Pages 883-891

  Burford, Michele A ^a   Davis, Timothy W ^a  

^a GRIFFITH UNIVERSITY   (Australia)

Author keywords

algal toxins; cyanobacteria; freshwater; light; nutrients; temperature

Indexed keywords

ALGAE; CYANOBACTERIA; CYLINDROSPERMOPSIS; CYLINDROSPERMOPSIS RACIBORSKII;

EID: 82055185386     PISSN: 02544059     EISSN: 19935005     Source Type: Journal    
DOI: 10.1007/s00343-011-0517-5     Document Type: Review

References (94)

1. Antenucci J, Ghanouani A, Burford M, Romero J. 2005. The impact of artificial destratification on phytoplankton species composition in a sub-tropical reservoir. Freshwater Biol., 50: 1 081-1 093.
2. Banker R, Carmeli S, Hadas O, Teltsch B, Porat R, Sukenik A. 1997. Identification of cylindrospermopsin in Aphanizomenon ovalisporum (Cyanophyceae) isolated from Lake Kinneret. Isr. J. Phycol., 33: 613-616.
3. Baxa D V, Kurobe T, Ger K A, Lehman P W, Teh S J. 2010. Estimating the abundance of toxic Microcystis in the San Francisco Estuary using quantitative real-time PCR. Harmful Algae, 9: 342-349.
4. Bouvy M, Molica R J R, De Oliveira S M, Marinho M, Beker B. 1999. Dynamics of a toxic cyanobacterial bloom (Cylindrospermopsis raciborskii) in a shallow reservoir in semiarid northeast, Brazil. Aquat. Microb. Ecol., 20: 285-297.
5. Bouvy M, Falcao D, Marinho M, Pagano M, Moura A. 2000. Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquat. Microb. Ecol., 23: 13-27.
6. Bouvy M, Ba N, Ka S, Sane S, Pagano M, Arfi R. 2006. Phytoplankton community structure and species assemblage succession in a shallow tropical lake (Lake Guiers, Senegal). Aquat. Microb. Ecol., 45: 147-161.
7. 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.
8. Branco C W C, Senna P A C. 1996. Relations among heterotrophic bacteria, chlorophyll-a, total phytoplankton, total zooplankton and physical and chemical features in the Paranoa reservoir, Brasilia, Brazil. Hydrobiologia, 337: 171-181.
9. Burford M A, O'Donohue M J. 2006. A comparison of phytoplankton community assemblages in artificial and naturally mixed subtropical water reservoirs. Freshwater Biol., 51: 973-982.
10. Burford M A, McNeale K L, McKenzie-Smith F J. 2006. The role of nitrogen in promoting Cylindrospermopsis raciborskii in a subtropical water reservoir. Freshwater Biol., 51: 2 143-2 153.
11. Burford M A, Johnston S A, Cook A J, Packer T V, Taylor B M, Townsley E R. 2007. Correlations between watershed and reservoir characteristics, and algal blooms in subtropical reservoirs. Water Res., 41: 4 105-4 114.
12. Chapman A D, Schelske C L. 1997. Recent appearance of Cylindrospermopsis (Cyanobacteria) in five hypereutrophic Florida lakes. J. Phycol., 33: 191-195.
13. Chonudomkul D, Yongmanitchai W, Theeragool G, Kawachi M, Kasai F, Kaya K, Watanabe M M. 2004. Morphology, genetic diversity, temperature tolerance and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan. FEMS Microbiol. Ecol., 48: 345-355.
14. Conroy J D, Quinlan E L, Kane D D, Culver D A. 2007. Cylindrospermopsis in Lake Erie: Testing its association with other cyanobacterial genera and major limnological parameters. J. Great Lakes Res., 33: 519-535.
15. Davis T W, Berry D L, Boyer G L, Gobler C J. 2009. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae, 8: 715-725.
16. Davis T W, Harke M J, Marcoval M A, Goleski J, Orano-Dawson C, Berry D L, Gobler C J. 2010. Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during bloom events. Aquat. Microb. Ecol., 61: 149-162.
17. Davis T W, Gobler C J. 2011. Grazing by mesozooplankton and microzooplankton on toxic and non-toxic strains of Microcystis in the Transquaking River, a tributary of Chesapeake Bay. J. Plankt. Res., 33: 415-430.
18. Dufour P, Sarazin G, Quiblier C, Sane S, Leboulanger C. 2006. Cascading nutrient limitation of the cyanobacterium Cylindrospermopsis raciborskii in a Sahelian lake (North Senegal). Aquat. Microbial Ecol., 44: 219-230.
19. Dyble J, Tester P A, Litaker R W. 2006. Effects of light intensity on cylindrospermopsin production in the cyanobacterial HAB species Cylindrospermopsis raciborskii. Afr. J. Mar. Sci., 28: 309-312.
20. Edwards D J, Marquez B L, Nogle L M, McPhail K, Goeger D E, Roberts M A, Gerwick W H. 2004. Structure and biosynthesis of the jamaicamides, new mixed polyketide-peptide neurotoxins from the marine cyanobacterium Lyngbya majuscule. Chem. Biol., 11: 817-833.
21. Fabbro L D, Duivenvoorden L J. 1996. Profile of a bloom of the cyanobacterium Cylindrospermopsis raciborskii (Woloszynska) Seenayya and Subba Raju in the Fitzroy River in tropical central Queensland. Mar. Freshwater Res., 47: 685-694.
22. Fastner J, Heinze R, Humpage A R, Mischke U, Eaglesham G K, Chorus I. 2003. Cylindrospermopsis occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii (Cyanobacteria) isolates. Toxicon, 42: 313-321.
23. Figueredo C C, Giani A. 2009. Phytoplankton community in the tropical lake of Lagoa Santa (Brazil): Conditions favouring a persistent bloom of Cylindrospermopsis raciborskii. Limnologica, 39: 264-272.
24. Ha J H, Hidaka T, Tsuno H. 2009. Quantification of toxic Microcystis and evaluation of its dominance ratio in blooms using Real-Time PCR. Environ. Sci. Technol., 43: 812-818.
25. Hamilton P B, Ley L M, Dean S, Pick F R. 2005. The occurrence of the cyanobacterium Cylindrospermopsis raciborskii in Constance Lake: an exotic cyanoprokaryote new to Canada. Phycologia, 44: 17-25.
26. Harada K, Ohtani I, Iwamoto K, Suzuki M, Watanabe M F, Watanabe M, Terao K. 1994. Isolation of cylindrospermopsin from a cyanobacterium Umezakia natans and its screening method. Toxicon, 32: 73-84.
27. Harris G P, Baxter G. 1996. Interannual variability in phytoplankton biomass and species composition in a subtropical reservoir. Freshwater Biol., 35: 545-560.
28. Havens K E, Philips E J, Cichra M F, Li B L. 1998. Light availability as a possible regulator of cyanobacterial species composition in a shallow subtropical lake. Freshwater Biol., 39: 547-556.
29. Hawkins P R, Runnegar M T C, Jackson A R B, Falconer I R. 1985. Severe hepatotoxicity caused by the tropical cyanobacterium Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated from a domestic water supply reservoir. Appl. Environ. Microbiol., 50: 1 292-1 295.
30. Hawkins P R, Putt E, Falconer I, Humpage A. 2001. Phenotypical variation in a toxic strain of the phytoplankter, Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) during batch culture. Environ. Toxicol., 16: 460-467.
31. Hong Y A, Steinman A, Biddanda B, Rediske R, Fahnenstiel G. 2006. Occurrence of the toxin-producing cyanobacterium Cylindrospermopsis raciborskii in Mona and Muskegon Lakes, Michigan. J. Great Lakes Res., 32: 645-652.
32. Hotto A M, Satchwell M F, Berry D L, Gobler C J, Boyer G L. 2008. Spatial and temporial diversity of microcystins and microcystin-producing genotypes in Oneida Lake, NY. Harmful Algae, 7: 671-681.
33. Humpage A R, Fenech M, Thomas P, Falconer I R. 2000. Micronucleus induction and chromosome loss in transformed human white cells indicate clastogenic and aneugenic action of the cyanobacterial toxin, cylindrospermopsin. Mutat. Res., 472: 155-161.
34. Isvánovics V, Shafik H M, Présing, Juhos S. 2000. Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshwater Biol., 43: 257-275.
35. Kehoe M. 2010. Modelling of Physical and Physiological Processes Controlling Primary Production and Growth in Toxic Filamentous Cyanobacteria. Ph. D. Thesis. University of Queensland, Australia.
36. Kellmann R, Mills T, Neilan B A. 2006. Functional modeling and phylogenetic distribution of putative cylindrospermopsin biosynthesis enzymes. J. Mol. Evol., 62: 267-280.
37. 2 fixation of Cylindrospermopsis raciborskii in phosphorus-limited chemostat cultures. Hydrobiologia, 623: 191-202.
38. Kiss T, Vehovszky A, Hiripi L, Kovacs A, Voros L. 2002. Membrane effects of toxins isolated from a cyanobacterium, Cylindrospermopsis raciborskii, on identified molluscan neurones. Comp. Biochem. Physiol. Part C, 131: 167-176.
39. Lagos N, Onodera H, Zagatto P A, Andrinolo D, Azevedo S M F Q, Oshima Y. 1999. The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon, 37: 1 359-1 373.
40. Li R H, Carmichael W W, Brittain S, Eaglesham G K, Shaw G R, Liu Y D, Watanabe M M. 2001a. First report of the cyanotoxins cylindrospermopsin and deoxycylindrospermopsin from Raphidiopsis curvata (cyanobacteria). J. Phycol., 37: 1 121-1 126.
41. Li R H, Carmichael W W, Brittain S, Eaglesham G K, Shaw G R, Mahakhant A, Noparatnaraporn N, Yongmanitchai W, Kaya K, Watanabe M M. 2001b. Isolation and identification of the cyanotoxin cylindrospermopsin and deoxy-cylindrospermopsin from a Thailand strain of Cylindrospermopsis raciborskii (cyanobacteria). Toxicon, 39: 973-980.
42. Lindenschmidt K E. 1999. Controlling the growth of Microcystis using surged artificial aeration. International Revue of Hydrobiology, 84: 243-254.
43. Messineo V, Melchiorre S, Di Corcia A, Gallo P, Bruno M. 2010. Seasonal succession of Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum blooms with cylindrospermopsin occurrence in the volcanic Lake Albano, central Italy. Environ. Toxicol., 25: 18-27.
44. Mihali T K, Kellmann R, Muenchhoff J, Barrow K D, Neilan B A. 2008. Characterization of the gene cluster responsible for cylindrospermopsin biosynthesis. Appl. Environ. Microbiol., 74: 716-722.
45. McGregor G B, Fabbro L D. 2000. Dominance of Cylindrospermopsis raciborskii (Nostocales, Cyanop tokaryota) in Queensland tropical and subtropical reservoirs: implications for monitoring and management. Lakes Res. Management, 5: 195-205.
46. McGregor G B, Sendall B C, Hunt L T, Eaglesham G K. 2011. Report of the cyanotoxins cylindrospermopsin and deoxy-cylindrospermopsin from Raphidiopsis mediterranea Skuja (Cyanobacteria/Nostocales). Harmful Algae, 10: 402-410.
47. Moffitt M C, Neilan B A. 2004. Characterization of the nodularin synthetase gene cluster and proposed theory of the evolution of cyanobacterial hepatotoxins. Appl. Environ. Microbiol., 70: 6 353-6 362.
48. Mohamed Z A. 2007. First report of toxic Cylindrospermopsis raciborskii and Raphidiopsis mediterranea (Cyanoprokaryota) in Egyptian fresh waters. FEMS Microbiol. Ecol., 59: 749-761.
49. Moisander P H, Paerl H W, Zehr J P. 2008. Effects of inorganic nitrogen on taxa-specific cyanobacterial growth and nifH expression in a subtropical estuary. Limnol. Oceanogr., 53: 2 519-2 522.
50. Moisander P H, Ochiai M, Lincoff A. 2009a. Nutrient limitation of Microcystis aeruginosa in northern California Klamath River reservoirs. Harmful Algae, 8: 889-897.
51. Moisander P H, Lehman P W, Ochiai M, Corum S. 2009b. Diversity of Microcystis aeruginosa in the Kalamath River and San Fancisco Bay delta, California, USA. Aquat. Microb. Ecol., 57: 19-31.
52. Neilan B A, M Saker L, Fastner J, Torokne A, Burns B P. 2003. Phylogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii. Mol. Ecol., 12: 133-140.
53. Norris R L, Eaglesham G K, Pierens G, Shaw G R, Smith M J, Chiswell R K, Seawright A A, Moore M R. 1999. Deoxycylindrospermopsin, an analog of cylindrospermopsin from Cylindrospermopsis raciborskii. Environ. Toxicol., 14: 163-165.
54. Oberholster P J, Botha A M, Cloete T E. 2006. Use of molecular markers as indicators for winter zooplankton grazing on toxic benthic cyanobacteria colonies in an urban Colorado lake. Harmful Algae, 5: 705-716.
55. O'Brien K R, Burford M A, Brookes J D. 2009. Effects of light history on primary productivity in a Cylindrospermopsis raciborskii-dominated reservoir. Freshwater Biol., 54: 272-282.
56. Ohtani I, Moore R E, Runnegar M T C. 1992. Cylindrospermopsin: a potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii. J. Amer. Chem. Soc., 114: 7 942-7 944.
57. Orr P T, Jones G J. 1998. Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnol. Oceanogr., 43: 1 604-1 614.
58. Orr P T, Rasmussen J P, Burford M A, Eaglesham G K, Lennox S M. 2010. Evaluation of quantitative real-time PCR to characterise spatial and temporal variations in cyanobacteria, Cylindrospermopsis raciborskii (Woloszynska) Seenaya et Subba Raju and cylindrospermopsin concentrations in three subtropical Australian reservoirs. Harmful Algae, 9: 243-254.
59. Padisák J. 1997. Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Arch. Hydrobiol. Suppl., 107: 563-593.
60. Padisák J, Istvanovics V. 1997. Differential response of blue-green algal groups to phosphorus load reduction in a large shallow lake: Balaton, Hungary. International Association of Theoretical and Applied Limnology Proceedings, 26: 574-580.
61. Paerl H W, Huisman J. 2008. Climate-Blooms like it hot. Science, 320: 57-58.
62. Posselt A J. 2010. Are Nutrients the Key Driver in Promoting Dominance of Toxic Cyanobacterial Blooms in a Sub-tropical Reservoir? Ph. D. Thesis. Griffith University, Queensland, Australia.
63. Posselt A J, Burford M A, Shaw G. 2009. Pulses of phosphate promote dominance of the toxic cyanophyte Cylindrospermopsis raciborskii in a subtropical water reservoir. J. Phycol., 45: 540-546.
64. Preußel K, Stuken A, Wiedner C, Chorus I, Fastner J. 2006. First report on cylindrospermopsin producing Aphanizomenon flos-aquae (Cyanobacteria) isolated from two German lakes. Toxicon, 47: 156-162.
65. Preußel K, Wessel G, Fastner J, Chorus I. 2009. Response of cylindrospermopsin production and release in Aphanizomenon flos-aquae (Cyanobacteria) to varying light and temperature conditions. Harmful Algae, 8: 645-650.
66. Présing M, Herodek S, Vörös L, Kóbor I. 1996. Nitrogen fixation, ammonium and nitrate uptake during a bloom of Cylindrospermopsis raciborskii in Lake Balaton. Archiv Hydrobiologia, 136: 553-562.
67. Quiblier C, Leboulanger C, Sané S, Dufour P. 2008. Phytoplankton growth control and risk of cyanobacterial blooms in the lower Senegal River delta region. Water Res., 42: 1 023-1 034.
68. 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: 1 503-1 515.
69. Reynolds C S, Huszar V, Kruk C, Naselli-Flores L, Melo S. 2002. Towards a functional classification of the freshwater phytoplankton. J. Plankton Res., 24: 417-428.
70. Rinta-Kanto J M, Ouellette A J A, Boyer G L, Twiss M R, Bridgeman T B, Wilhelm S W. 2005. Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in western Lake Erie using quantitative real-time PCR. Environ. Sci. Technol., 39: 4 198-4 205.
71. Rinta-Kanto J M, Wilhelm S W. 2006. Diversity of microcystin-producing cyanobacteria in spatially isolated regions of Lake Erie. Appl. Environ. Microbiol., 72: 5 083-5 085.
72. Rinta-Kanto J M, Konopko E, DeBruyn J M, Bourbonniere R A, Boyer G L, Wilhelm S W. 2009a. Lake Erie Microcystis: Relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae, 8: 665-673.
73. Rinta-Kanto J M, Saxton M A, DeBruyn J M, Smith J L, Marvin C H, Krieger K A, Sayler G S, Boyer G L, Wilhelm S W. 2009b. The diversity and distribution of toxigenic Microcystis spp. in present day and archived pelagic and sediment samples from Lake Erie. Harmful Algae, 8: 385-394.
74. Robarts R D, Zohary T. 1987. Temperature effects on photosynthetic capacity, respiration, and growth rates of bloom-forming cyanobacteria. New Zeal. J. Mar. Freshwater Res., 21: 391-399.
75. Runnegar M T, Kong S M, Zhong Y Z, Ge J L, Lu S C. 1994. The role of glutathione in the toxicity of a novel cyanobacterial alkaloid cylindrospermopsin in cultured rat hepatocytes. Biochemical and Biophysical Research Communications, 201: 235-241.
76. Runnegar M T, Kong S M, Zhong Y Z, Lu S C. 1995. Inhibition of reduced glutathione synthesis by cyanobacterial alkaloid cylindrospermopsin in cultured rat hepatocytes. Biochem. Pharmacol., 49: 219-225.
77. Runnegar M T, Xie C, Snider B B, Wallace G A, Weinreb S M, Kuhlenkamp J. 2002. In vitro hepatotoxicity of the cyanobacterial alkaloid cylindrospermopsin and related synthetic analogues. Toxicol. Sci., 67: 81-87.
78. Saker M L. 2000. Cyanobacterial Blooms in Tropical North Queensland Water Bodies. Ph. D. Thesis. James Cook University, Townsville, Australia.
79. Saker M L, Neilan B A, Griffiths D J. 1999. Two morphological forms of Cylindrospermopsis raciborskii (cyanobacteria) isolated from Solomon Dam, Palm Island, Queensland. J. Phycol., 35: 599-606.
80. Saker M L, Griffiths D J. 2000. The effect of temperature on growth and cylindrospermopsin content of seven isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from water bodies in northern Australia. Phycologia, 39: 349-354.
81. Saker M L, Neilan B A. 2001. Varied diazotrophies, morphologies, and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from northern Australia. Appl. Microbiol., 67: 1 839-1 845.
82. Saker M L, Nogueira I R, Vasconcelos V M, Neilan B A, Eaglesham G K, Pereira P. 2003. First report and toxicological assessment of the cyanobacterium Cylindrospermopsis raciborskii from Portuguese freshwaters. Ecotoxicol. Environ. Saf., 55: 243-250.
83. Schembri M A, Neilan B A, Saint C P. 2001. Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environ. Toxicol., 16: 413-421.
84. Seifert M, McGregor G, Eaglesham G, Wickramasinghe W, Shaw G. 2007. First evidence for the production of cylindrospermopsin and deoxy-cylindrospermopsin by the freshwater benthic cyanobacterium, Lyngbya wollei (Farlow ex Gomont) Speziale and Dyck. Harmful Algae, 6: 73-80.
85. Shafik H M, Herodek S, Présing M, Voros L. 2001. Factors affecting growth and cell composition of cyanoprokaryote Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju. Algological Studies, 103: 74-103.
86. Spröber P, Shafik H M, Présing M, Kovács A W, Herodek S. 2003. Nitrogen uptake and fixation in the cyanobacterium Cylindrospermopsis raciborskii under different nitrogen conditions. Hydrobiologia, 506-509: 169-174.
87. Tillett D, Dittmann E, Erhard M, von Dohren H, Borner T, Neilan B A. 2000. Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: An integrated peptide-polyketide synthetise system. Chem. Biol., 7: 753-764.
88. Vézie C, Rapala J, Vaitomaa J, Seitsonen J, Sivonen K. 2002. Effect of nitrogen and phosphorus on growth of toxic and nontoxic Microcystis strains and on intracellular microcystin concentrations. Microb. Ecol., 43: 443-454.
89. Visser P M, Ibelings B W, van Der Veer B, Koedood J, Mur L R. 1996. Artificial mixing prevents nuisance blooms of the cyanobacterium Microcystis in Lake Nieuwe Meer, the Netherlands. Freshwater Biol., 36: 435-450.
90. Wiedner C, Rücker J, Brüggemann R, Nixdorf B. 2007. Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions. Oecologia, 152: 473-484.
91. Wiedner C, Rücker J, Fastner J, Chorus I, Nixdorf B. 2008. Seasonal changes of cylindrospermopsin and cyanobacteria in two German lakes. Toxicon, 52: 677-686.
92. Wood S A, Stirling D J. 2003. First identification of the cylindrospermopsin producing cyanobacterium Cylindrospermopsis raciborskii in New Zealand. New Zeal. J. Mar. Freshwater Res., 37: 821-828.
93. Ye W, Liu X, Tan J, Li D, Yang H. 2009. Diversity and dynamics of microcystin-producing cyanobacteria in China's third largest lake, Lake Taihu. Harmful Algae, 8: 637-644.
94. Yi{dotless}lmaz 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.