Cylindrospermopsin and Saxitoxin Synthetase Genes in Cylindrospermopsis raciborskii Strains from Brazilian Freshwater

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Hoff Risseti, Caroline ^a   Dörr, Felipe Augusto ^a   Schaker, Patricia Dayane Carvalho ^a   Pinto, Ernani ^a   Werner, Vera Regina ^b   Fiore, Marli Fatima ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Natural Sciences Museum   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CYLINDROSPERMOPSIN; FRESH WATER; SAXITOXIN;

ARTICLE; ASIA; AUSTRALIA; BACTERIAL STRAIN; BACTERIUM CULTURE; BOOTSTRAPPING; BRAZILIAN; CYLINDROSPERMOPSIS RACIBORSKII; CYRA GENE; CYRB GENE; CYRC GENE; CYRJ GENE; ETHNIC GROUP; GENE; GENE SEQUENCE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN DOMAIN; PROTEIN FUNCTION; SAXITOXIN SYNTHETASE GENE; SOUTH AMERICA; SXTA GENE; SXTB GENE; SXTI GENE; UNINDEXED SEQUENCE;

BACTERIAL PROTEINS; BRAZIL; CYLINDROSPERMOPSIS; FRESH WATER; LIGASES; SAXITOXIN; SPECIES SPECIFICITY; URACIL; WATER MICROBIOLOGY;

EID: 84883157094     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074238     Document Type: Article

References (85)

1. Seenayya G, Subba Raju N (1972) On the ecology and systematic position of the algae known as Anabaenopsis raciborskii (Wolosz) Elenkin and a critical evaluation of the forms described under the genus Anabaenopsis. In: Desikachary, TV (1972) Taxonomy and Biology of Blue-green Algae. India: University of Madras. pp 52-57.
2. Hoffmann L, Komárek J, Kaštovský J, (2005) System of cyanoprokaryotes (Cyanobacteria): state in 2004. Algol Stud 117: 95-115.
3. Komárek J, Hauer T (2013) CyanoDBcz: On-line database of cyanobacterial genera University of South Bohemia and Institute of Botany AS CR. Available: http://www.cyanodb.cz. Accessed 25 March 2013.
4. Hawkins PR, Chandrasena NR, Jones GJ, Humpage AR, Falconer IR, (1997) Isolation and toxicity of Cylindrospermopsis raciborskii from an ornamental lake. Toxicon 35: 341-346.
5. Castenholz RW (2001) Phylum BX Cyanobacteria oxygenic photosynthetic bacteria. In: Boone DR, Castenholz RW, Garrity GM, eds. Bergey's manual of systematic bacteriology. New York: Springer-Verlag. pp 474-599.
6. Hawkins PR, Runnegar MTC, Jackson ARB, Falconer IR, (1985) Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green-alga) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated from a domestic water-supply reservoir. Appl Environ Microbiol 50: 1292-1295.
7. Lagos N, Onodera H, Zagatto PA, Andrinolo D, Azevedo SMFQ, et al. (1999) The first evidence of paralytic shellfish toxins in the fresh water cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon 37: 1359-1373.
8. Dittmann E, Fewer DP, Neilan BA, (2012) Cyanobacterial toxins: biosynthetic routes and evolutionary roots. FEMS Microbiol Rev 37: 23-43.
9. Terao K, Ohmori S, Igarashi K, Ohtani I, Watanabe MF, et al. (1994) Electron microscopic studies on experimental poisoning in mice induced by cylindrospermopsin isolated from blue-green alga Umezakia natans. Toxicon 32: 833-843.
10. Humpage AR, Fenech M, Thomas P, Falconer IR, (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.
11. Froscio SM, Humpage AR, Burcham PC, Falconer IR, (2003) Cylindrospermopsin induced protein synthesis inhibition and its dissociation from acute toxicity in mouse hepatocytes. Environ Toxicol 18: 243-251.
12. Mihali TK, Kellmann R, Muenchhoff J, Barrow KD, Neilan BA, (2008) Characterization of the gene cluster responsible for cylindrospermopsin biosynthesis. Appl Environ Microbiol 74: 716-722.
13. Wang J, Salata JJ, Bennett PB, (2003) Saxitoxin is a gating modifier of HERG K+ channels. J Gen Physiol 121: 583-598.
14. Su Z, Sheets M, Ishida H, Li F, Barry WH, (2004) Saxitoxin blocks L-type Ica. J Pharmacol Exp Ther 308: 324-329.
15. Padisák J, (1997) Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptative cyanobacterium: worldwide distribution and review of its ecology. Arch Hydrobiol 107: 563-593.
16. Sant'Anna CL, Azevedo MTP, (2000) Contribution to the knowledge of potentially toxic Cyanobacteria from Brazil. Nova Hedwigia 71: 359-385.
17. Briand JF, Robillot C, Quiblier-Lloberas C, Humbert JF, Couté A, et al. (2002) Environmental context of Cylindrospermopsis raciborskii (Cyanobacteria) blooms in a shallow pond in France. Water Res 36: 3183-3192.
18. 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.
19. Sinha R, Pearson LA, Davis TW, Burford MA, Orr PT, et al. (2012) Increased incidence of Cylindrospermopsis raciborskii in temperate zones- Is climate change responsible? Water Res 46: 1408-1419.
20. Branco CWC, Senna PAC, (1991) The taxonomic elucidation of the Paranoá Lake (Brasilia, Brazil) problem: Cylindrospermopsis raciborskii. Bull Jard Bot Nat Belg 61: 85-91.
21. de Souza RCR, Carvalho MC, Truzzi AC, (1998) Cylindrospermopsis raciborskii (Wolosz) Seenaya and Subba Raju (Cyanophyceae) dominance and a contribution to the knowledge of Rio Pequeno arm, Billings Reservoir, Brazil. Environ Toxicol Water Qual 13: 73-81.
22. Komárková J, Laudares-Silva R, Senna PAC, (1999) Extreme morphology of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in the Lagoa do Peri, a freshwater coastal lagoon, Santa Catarina, Brazil. Algol Stud 94: 207-222.
23. Bouvy M, Falcão 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.
24. Tucci A, Sant'Anna CL, (2003) Cylindrospermopsis raciborskii (Woloszynska) Seenayya and Suba Raju (Cyanobacteria): weekly variation and relation with environmental factors in an eutrophic lake, São Paulo, SP, Brazil. Rev Bras Bot 26: 97-112.
25. Yunes JS, Cunha NT, Proença LA, Monserrat JM, (2003) Cyanobacterial neurotoxins from Southern Brazilian Freshwaters. Comm Toxicol 9: 103-115.
26. Costa IAS, Azevedo SMFO, Senna PAC, Bernardo RR, Costa SM, et al. (2006) Occurrence of toxin-producing cyanobacteria blooms in a Brazilian semiarid reservoir. Braz J Biol 66: 211-219.
27. Carvalho LR, Pipole F, Werner VR, Laughinghouse HD, de Camargo ACM, et al. (2008) A toxic cyanobacterial bloom in an urban coastal lake, Rio Grande do Sul State, Southern Brazil. Braz J Microbiol 39: 761-769.
28. Gemelgo MCP, Sant'Anna CL, Tucci A, Barbosa HR, (2008) Population dynamics of Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju, a Cyanobacteria toxic species, in water supply reservoirs in São Paulo, Brazil. Hoehnea 35: 297-307.
29. Figueredo CC, Giani A, (2009) Phytoplankton community in the tropical lake of Lagoa Santa (Brazil): conditions favoring a persistent bloom of Cylindrospermopsis raciborskii. Limnol 39: 264-272.
30. Moschini-Carlos V, Bortoli S, Pinto E, Nishimura PY, de Freitas LG, et al. (2009) Cyanobacteria and cyanotoxin in the Billings reservoir (São Paulo, SP, Brazil). Limnetica 28: 273-282.
31. Soares MCS, Rocha MIA, Marinho MM, Azevedo SMFO, Branco CWC, et al. (2009) Changes in species composition during annual cyanobacterial dominance in a tropical reservoir: physical factors, nutrients and grazing effects. Aquat Microb Ecol 57: 137-149.
32. Huszar VLM, Silva LHS, Marinho M, Domingos P, Sant'Anna CL, (2000) Cyanoprokariote assemblage in eight productive tropical Brazilian waters. Hydrobiology 424: 67-77.
33. Couté A, Bouvy M, (2004) A new species of the genus Cylindrospermopsis, C acuminato-crispa spec. nova (Cyanophyceae, Nostocales) from Ingazeira reservoir, Northeast Brazil. Algol Stud 113: 57-72.
34. Zagatto PA (1998) Toxicity of the algae Cylindrospermopsis raciborskii isolated from Billings reservoir, Taquacetuba branch Technical Report, September 1998 Environmental Agency of São Paulo State (CETESB), São Paulo, SP, pp 23.
35. Saker ML, Thomas AD, Norton JH, (1999) Cattle mortality attributed to the toxic cyanobacterium Cylindrospermopsis raciborskii in an outback region of north Queensland. Environ Toxicol 14: 179-182.
36. Li R, Carmichael WW, Brittain S, Eaglesham GK, Shaw GR, et al. (2001b) First report of the cyanotoxins cylindrospermopsin and deoxycylindrospermopsin from Raphidiopsis curvata (Cyanobacteria). J Phycol 37: 1121-1126.
37. Wood SA, Stirling DJ, (2003) First identification of the cylindrospermopsin-producing cyanobacterium Cylindrospermopsis raciborskii in New Zealand. N Z J Mar Freshw Res 37: 821-828.
38. Chonudomkul D, Yongmanitchai W, Theeragool G, Kawachi M, Kasai F, et al. (2004) Morphology, genetic diversity, temperature tolerant and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan. FEMS Microbiol Ecol 48: 345-355.
39. Everson S, Fabbro L, Susan 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.
40. Kellmann R, Mihali TK, Jeon YJ, Pickford R, Pomati F, et al. (2008) Biosynthetic intermediate analysis and functional homology reveal a saxitoxin gene cluster in cyanobacteria. Appl Environ Microbiol 74: 4044-4053.
41. Molica R, Onodera H, García C, Rivas M, Andrinolo D, et al. (2002) Toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii (Cyanophyceae) isolated from Tabocas reservoir in Caruaru, Brazil, including demonstration of a new saxitoxin analogue. Phycologia 41: 606-611.
42. Ferrão-Filho AS, Cunha R, Magalhães VF, Soares MCS, Baptista DF, (2007) Evaluation of sub-lethal toxicity of cyanobacteria on the swimming activity of aquatic organisms by image analysis. J Braz Soc Ecotoxicol 2: 93-100.
43. Carmichael WW, Azevedo SMFO, An JS, Molica RJR, Jochimsen EM, et al. (2001) Human Fatalities from Cyanobacteria: Chemical and Biological Evidence for Cyanotoxins. Environ Health Persp 109: 663-668.
44. Bittencourt-Oliveira MC, Piccin-Santos V, Kujbida P, Moura AN, (2011) Cylindrospermopsin in water supply reservoirs in Brazil determined by immunochemical and molecular methods. J Water Res Protec 3: 349-355.
45. Schembri MA, Neilan BA, Saint CP, (2001) Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environ Toxicol 16: 413-421.
46. Muenchhoff J, Siddiqui KS, Poljak A, Raftery MJ, Barrow KD, (2010) A novel prokaryotic L-arginine:glycine amidinotransferase is involved in cylindrospermopsin biosynthesis. FEBS Journal 277: 3844-3860.
47. Gorham PR, McLahlan JR, Hammer VT, Kim WK, (1964) Isolation and culture of toxic strains of Anabaena flos-aquae (Lyngb) de Bréb Verh int Verein. Theor Angew Limnol 15: 796-804.
48. Cronberg G, Annadotter H (2006) Manual on aquatic cyanobacteria: a photo guide and a synopsis of their toxicology. International Society for the Study of Harmful AlgaeUnited Nations Educational, Scientific and Cultural Organization, Copenhagen. 106 p.
49. Fiore MF, Moon DH, Tsai SM, Lee H, Trevors JT, (2000) Miniprep DNA isolation from unicellular and filamentous cyanobacteria. J Microbiol Meth 39: 159-169.
50. Mazmouz R, Chapuis-Hugon F, Mann S, Pichon V, Méjean A, et al. (2010) Biosynthesis of cylindrospermopsin and 7-epicylindrospermopsin in Oscillatoria sp strain PCC 6506: identification of the cyr gene cluster and toxin analysis. Appl Environ Microbiol 76: 4943-4949.
51. Kellmann R, Mills T, Neilan BA, (2006) Functional modeling and phylogenetic distribution of putative cylindrospermopsin biosynthesis Enzymes. J Mol Evol 62: 267-280.
52. Birnboim HC, Doly J, (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7: 1513-1518.
53. Fiore MF, Sant'Anna CL, Azevedo MTP, Komárek J, Kaštovský J, (2007) The cyanobacterial genus Brasilonema, gen. nov., a molecular and phenotypic evaluation. J Phycol 43: 789-798.
54. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
55. Dörr FA, Tomaz JC, Lopes NP, Pinto E, (2008) Comparative analysis of the gas-phase reactions of cylindrospermopsin and the difference in the alkali metal cation mobility. Rapid Commun Mass Sp 22: 2015-2020.
56. Diener M, Erler K, Hiller S, Christian B, Luckas B, (2006) Determination of Paralytic Shellfish Poisoning (PSP) toxins in dietary supplements by application of a new HPLC/FD method. Eur Food Res Technol 224: 147-151.
57. Diener M, Erler K, Christian B, Luckas B, (2007) Application of a new zwitterionic hydrophillic interaction chromatography column for determination of paralytic shellfish poisoning toxins. J Sep Sci 30: 1821-1826.
58. Soto-Liebe K, Murillo AA, Krock B, Stucken K, Fuentes-Valdés JJ, et al. (2010) Reassessment of the toxin profile of Cylindrospermopsis raciborskii T3 and function of putative sulfotransferases in synthesis of sulfated and sulfonated PSP toxins. Toxicon 56: 1350-1361.
59. Dörr FA, Kovačević B, Maksić ZB, Pinto E, Volmer DA, (2011) Intriguing differences in the gas-phase dissociation behavior of protonated and deprotonated gonyautoxin epimers. J Am Soc Mass Spectro 22: 2011-2020.
60. Jiang Y, Xiao P, Yu G, Sano T, Pan Q, et al. (2012) Molecular basis and phylogenetic implications of deoxycylindrospermopsin biosynthesis in the cyanobacterium Raphidiopsis curvata. Appl Environ Microbiol 78: 2256-2263.
61. Stucken K, John U, Cembella A, Murillo AA, Soto-Liebe K, et al. (2010) The smallest known genomes of multicellular and toxic cyanobacteria: comparison, minimal gene sets for linked traits and the evolutionary implications. PLoS One 5: e9235.
62. Orr RJS, Stüken A, Murray SA, Jakobsen KS, (2013) Evolutionary acquisition and loss of saxitoxin biosynthesis in dinoflagellates: the second "core" gene, sxtG. Appl Environ Microbiol 79: 2128-2136.
63. Muenchhoff J, Siddiqui KS, Neilan BA, (2012) Identification of two residues essential for the stringent substrate specificity and active site stability of the prokaryotic L-arginine:glycine amidinotransferase CyrA. FEBS Journal 279: 805-815.
64. Loewe L, Cutter AD, (2008) On the potential for extinction by Muller's Ratchet in Caenorhabditis elegans. BMC Evol Biol 8: 125.
65. Ohtani I, Moore RE, Runnegar MTC, (1992) Cylindrospermopsin: A potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii. J Am Chem Soc 114: 7942-7944.
66. Banker R, Teltsch B, Sukenik A, Carmeli S, (2000) 7-epicylindrospermopsin, a toxic minor metabolite of the cyanobacterium Aphanizomenon ovalisporum from Lake Kinneret, Israel. J Nat Prod 63: 387-389.
67. Li R, Carmichael WW, Brittain S, Eaglesham GK, Shaw GR, et al. (2001a) Isolation and identification of the cyanotoxin cylindrospermopsin and deoxy-cylindrospermopsin from a Thailand strain of Cylindrospermopsis raciborskii (Cyanobacteria). Toxicon 39: 973-980.
68. Ballot A, Ramm J, Rundberget T, Kaplan-Levy RN, Hadas O, et al. (2011) Occurrence of non-cylindrospermopsin producing Aphanizomenon ovalisporum and Anabaena bergii in Lake Kinneret (Israel). J Plankton Res 33: 1736-1746.
69. Stucken K, Murillo AA, Soto-Liebe K, Fuentes-Valdés JJ, Méndez MA, (2009) Toxicity phenotype does not correlate with phylogeny of Cylindrospermopsis raciborskii strains. Syst Appl Microbiol 32: 37-48.
70. Moustafa A, Loram JE, Hackett JD, Anderson DM, Plumley FG, et al. (2009) Origin of saxitoxin biosynthetic genes in cyanobacteria. PLoS ONE 4: e5758.
71. Stüken A, Jakobsen KS, (2010) The cylindrospermopsin gene cluster of Aphanizomenon sp. strain 10E6: organization and recombination. Microbiol 156: 2438-2451.
72. Hackett JD, Wisecaver JH, Brosnahan ML, Kulis DM, Anderson DM, et al. (2012) Evolution of Saxitoxin Synthesis in Cyanobacteria and dinoflagellates. Mol BioL Evol 30: 70-78.
73. Soto-Liebe K, Méndez MA, Fuenzalida L, Krock B, Cembella A, et al. (2012) PSP toxin release from the cyanobacterium R. brookii D9 (Nostocales) can be induced by sodium and potassium ions. Toxicon 60: 1324-1334.
74. Fastner J, Heinze R, Humpage AR, Mischke U, Eaglesham GK, et al. (2003) Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii (Cyanobacteria) isolates. Toxicon 42: 313-321.
75. Neilan BA, Saker ML, Fastner J, Törökné A, Burns BP, (2003) Phylogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii. Mol Ecol 12: 133-140.
76. Yilmaz M, Phlips EJ, Szabo NJ, Badylak S, (2008) A comparative study of Florida strains of Cylindrospermopsis and Aphanizomenon for cylindrospermopsin production. Toxicon 51: 130-139.
77. Yilmaz M, Phlips EJ, (2011) Diversity of and selection acting on cylindrospermopsin cyrB gene adenylation domain Sequences in Florida. Appl Environ Microbiol 77: 2502-2507.
78. Preuβel K, Stüken 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.
79. Wormer L, Cires S, Carrasco D, Quesada A, (2008) Cylindrospermopsin is not degraded by co-occurring natural bacterial communities during a 40-day study. Harmful Algae 7: 206-213.
80. Spoof L, Berg KA, Rapala J, Lahti K, Lepistö L, et al. (2006) First observation of cylindrospermopsin Anabaena lapponica isolated from the boreal environment (Finland). Environ Toxicol 21: 552-560.
81. Dyble J, Paerl HW, Neilan BA, (2002) Genetic characterization of Cylindrospermopsis raciborskii (Cyanobacteria) isolates from diverse geographic origins based on nifH and cpcBA-IGS nucleotide sequence analysis. Appl Environ Microbiol 68: 2567-2571.
82. Gugger M, Molica R, Le Berre B, Dufour P, Bernard C, (2005) Genetic diversity of Cylindrospermopsis strains (Cyanobacteria) isolated from four continents. Appl Environ Microbiol 71: 1097-1100.
83. Piccini C, Aubriot L, Fabre A, Amaral V, González-Piana M, et al. (2011) Genetic and eco-physiologycal differences of South American Cylindrospermopsis raciborskii isolates support the hypothesis of multiple ecotypes. Harmful Algae 10: 644-653.
84. Bahl J, Lau MCY, Smith GJD, Vijaykrishna D, Cary SC, et al. (2011) Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat Commun 2: 163.
85. van Gremberghe I, Leliaert F, Mergeay J, Vanormelingen P, Van der Gucht K, et al. (2011) Lack of phylogeographic structure in the freshwater cyanobacterium Microcystis aeruginosa suggests global dispersal. PLoS One 6: e19561.