Application of real-time PCR in the assessment of the toxic cyanobacterium Cylindrospermopsis raciborskii abundance and toxicological potential

Applied Microbiology and Biotechnology

Volumn 92, Issue 1, 2011, Pages 189-197

  Moreira, Cristiana ^a,b   Martins, António ^a   Azevedo, Joana ^a,c   Freitas, Marisa ^a,d   Regueiras, Ana ^a   Vale, Micaela ^a   Antunes, Agostinho ^a   Vasconcelos, Vitor ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c Escola Superior de Tecnologia da Saúde do Porto   (Portugal)

^d POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

Author keywords

C. raciborskii; Cylindrospermopsin genes; Monitoring; Real time PCR

Indexed keywords

16S RRNA; AQUATIC ENVIRONMENTS; C. RACIBORSKII; CYANOBACTERIUM; CYLINDROSPERMOPSIN; CYTOTOXIC; GENETIC MARKERS; IN-FIELD; PHOTOSYNTHETIC MICROORGANISMS; PORTUGAL; REAL-TIME PCR; SEASONAL VARIATION; SHALLOW PONDS; SYNTHETASES; TEMPERATE REGIONS; TOXIC CYANOBACTERIUM; TOXIN PRODUCTION;

ENVIRONMENTAL IMPACT; GENES; LAKES; METABOLITES; MONITORING; RNA; TOXIC MATERIALS;

POLYMERASE CHAIN REACTION;

CYLINDROSPERMOPSIN SYNTHETASE; RNA 16S; SYNTHETASE; UNCLASSIFIED DRUG;

ABUNDANCE; AGRICULTURAL PRACTICE; AQUATIC ENVIRONMENT; CATTLE; CYANOBACTERIUM; ECOTOXICOLOGY; ENVIRONMENTAL IMPACT; ENVIRONMENTAL MONITORING; GENETIC MARKER; MORBIDITY; MORTALITY; POLYMERASE CHAIN REACTION; POPULATION DYNAMICS; REAL TIME; RECREATIONAL ACTIVITY; SEASONAL VARIATION; TOXIC ORGANISM; TOXICITY TEST; TOXIN;

AQUATIC ENVIRONMENT; ARTICLE; BACTERIAL GENE; BACTERIUM DETECTION; CYLINDROSPERMOPSIS; CYLINDROSPERMOPSIS RACIBORSKII; GENETIC MARKER; GENETIC VARIABILITY; NONHUMAN; POPULATION DYNAMICS; REAL TIME POLYMERASE CHAIN REACTION; SEASONAL VARIATION; TOXICOLOGY;

BACTERIAL PROTEINS; BACTERIOLOGICAL TECHNIQUES; CYLINDROSPERMOPSIS; DNA PRIMERS; DNA, BACTERIAL; DNA, RIBOSOMAL; LIGASES; PORTUGAL; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; URACIL; WATER MICROBIOLOGY;

COIMBRA [PORTUGAL]; PORTUGAL; VELA LAKE;

BOS; CYANOBACTERIA; CYLINDROSPERMOPSIS RACIBORSKII; PROKARYOTA;

EID: 82455188039     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3360-x     Document Type: Article

References (46)

1. Abrantes N, Pereira R, Gonçalves F (2006) First step for an ecological risk assessment to evaluate the impact of diffuse pollution in Lake Vela (Portugal). Environ Monit Assess 117:411-431 (Pubitemid 44255946)
2. Banker R, Carmeli S, Hadas O, Teltsch B, Porat R, Sukenik A (1997) Identification of cylindrospermopsin in the cyanobacterium Aphanizomenon ovalisporum (Cyanophyceae) isolated from Lake Kinneret. J Phycol 33:613-616 (Pubitemid 27383385)
3. Berry JP, Lind O (2010) First evidence of "paralytic shellfish toxins" and cylindrospermopsin in aMexican freshwater system, Lago Catemaco, and apparent bioaccumulation of the toxins in "tegogolo" snails (Pomacea patula catemacensis). Toxicon 55(5):930-938
4. Bláhová L, Oravec M, Maršálek B, Šejnohová L, Šimek Z, Bláha L (2009) The first occurrence of the cyanobacterial alkaloid toxin cylindrospermopsin in the Czech Republic as determined by immunochemical and LC/MS methods. Toxicon 53:519-524
5. Briand JF, Robillot C, Quiblier-Llobéras C, Humbert JF, Couté A, Bernard C (2002) Environmental context of Cylindrospermopsis raciborskii (Cyanobacteria) blooms in a shallow pond in France. Water Res 36:3183-3192 (Pubitemid 35291798)
6. Brient L, Lengronne M, Bormans M, Fastner J (2009) First occurrence of cylindrospermopsin in freshwater in France. Environ Toxicol 24(4):415-420
7. Bourke ATC, Hawes RB, Neilson A, Stallman ND (1983) An outbreak of hepato-enteritis (the Palm Island mystery disease) possibly caused by algal intoxication. Toxicon 21(Supplement 3):45-48
8. Chiswell R, Smith M, Norris R, Eaglesham G, Shaw G, Seawright A, Moore M (1997) The cyanobacterium, Cylindrospermopsis raciborskii, and its related toxin, cylindrospermopsin. Australas J Ecotoxicol 3:7-23
9. de Figueiredo DR, Reboleira ASSP, Antunes SC, Abrantes N, Azeiteiro U, Gonçalves F, Pereira MJ (2006) The effect of environmental parameters and cyanobacterial blooms on phytoplankton dynamics of a Portuguese temperate lake. Hydrobiologia 568:145-157 (Pubitemid 44174675)
10. de Figueiredo DR, Pereira MJ, Moura A, Silva L, Bárrios S, Fonseca F, Henriques I, Correia A (2007) Bacterial community composition over a dry winter in meso-And eutrophic Portuguese water bodies. FEMS Microbiol Ecol 59:638-650 (Pubitemid 46376238)
11. Falconer IR (2005) Cyanobacterial toxins of drinking water supplies. CRC, Boca Raton.
12. Falconer IR, Humpage AR (2001) Preliminary evidence for in vivo tumour initiation by oral administration of extracts of the bluegreen alga Cylindrospermopsis raciborskii containing the toxin cylindrospermopsin. Environ Toxicol 16:192-195 (Pubitemid 32294157)
13. Fastner J, Heinze R, Humpage AR, Mischke U, Eaglesham GK, Chorus I (2003) Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii (Cyanobacteria) isolates. Toxicon 42:313-321 (Pubitemid 37338169)
14. Fergusson KM, Saint PC (2003) Multiplex PCR assay for Cylindrospermopsis raciborskii and cylindrospermopsin-producing cyanobacteria. Environ Toxicol 18(2):120-125 (Pubitemid 44783329)
15. Freitas M (2009) Monitorização de cianobactérias e cianotoxinas nas lagoas Portuguesas de Mira e Vela comparando métodos moleculares, imunológicos e volumes de amostragem. Dissertation, University of Porto
16. Hamilton PB, Ley LM, Dean S, Pick FR (2005) The occurrence of the cyanobacterium Cylindrospermopsis raciborskii in Constance Lake, an exotic cyanoprokaryote new to Canada. Phycologia 44:17-25 (Pubitemid 40274197)
17. Harada K, Ohtani I, Iwamoto K, Suzuki M, Wantanabe MF, Wantanabe M, Terao K (1994) Isolation of cylindrospermopsin from a cyanobacterium Umezakia natans and its screening method. Toxicon 32:73-84 (Pubitemid 24047963)
18. 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 supply reservoir. Appl Environ Microbiol 50:1292-1295 (Pubitemid 16193446)
19. Humpage AR, Falconer IR (2003) Oral toxicity of the cyanobacterial toxin cylindrospermopsin in male Swiss albino mice: Determination of no observed adverse effect level for deriving a drinking water guideline value. Environ Toxicol 18(2):94-103 (Pubitemid 44783326)
20. 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
21. Kurmayer R, Kutzenberger T (2003) Application of real-Time PCR for quantification of microcystin genotypes in a population of the toxic cyanobacterium Microcystis sp. Appl Environ Microbiol 69 (11):6723-6730 (Pubitemid 37420210)
22. Lagos N, Onodera H, Zagatto PA, Andrinolo D, Azevedo SMFO, Oshima Y (1999) The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon 37:1359-1373 (Pubitemid 29264099)
23. Li R, Carmichael WW, Brittain S, Eaglesham GK, Shaw GR, Liu Y, Watanabe MM (2001) First report of the cyanotoxins cylindrospermopsin and deoxycylindrospermopsin from Raphidiopsis curvata (Cyanobacteria). J Phycol 37:1121-1126 (Pubitemid 34067670)
24. Manti G,Mattei D,MessineoV,Melchiorre S, Bogialli S, Sechi N, Casiddu P, Luglié L, Di Brizio M, Bruno M (2005) First report of Cylindrospermopsis raciborskii in Italy. Harmful Algal News 28:8-9
25. Neilan BA, Saker ML, Fastner J, Torokne A, Burnes BP (2003) Phylogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii. Mol Ecol 12:113-140
26. Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63 (8):3327-3332 (Pubitemid 27337840)
27. 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
28. Pearson LA, Neilan B (2008) The molecular genetics of cyanobacterial toxicity as a basis for monitoring water quality and public health risk. Curr Opin Biotechnol 19(3):281-288
29. Preußel K, Stüken A, Wiedner C, Chorus I, Fastner J (2006) First report on cylindrospermopsin producing Aphanizomenon flosaquae (Cyanobacteria) isolated from two German lakes. Toxicon 47:156-162 (Pubitemid 43143224)
30. Quesada A, Moreno E, Carrasco D, Paniagua T, Wormer L, De Hoyos C, Sukenik A (2006) Toxicity of Aphanizomenon ovalisporum (Cyanobacteria) in a Spanish water reservoir. Eur J Phycol 41:39-45 (Pubitemid 43379203)
31. Rasmussen JP, Giglio S, Monis PT, Campbell RJ, Saint SP (2007) Development and field testing of a real-Time PCR assay for cylindrospermopsin- producing cyanobacteria. J Appl Microbiol 104(5):1503-1515
32. Romo S, Miracle MR (1994) Population dynamics and ecology of subdominant phytoplankton species in a shallow hypertrophic lake (Albufera of Valencia, Spain). Hydrobiologia 273:37-56 (Pubitemid 2043947)
33. Rinta-Kanto JM, Ouellette AJA, Boyer GL, Twiss MR, Bridgeman TB, Wilhelm SW (2005) Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in western Lake Erie using quantitative real-Time PCR. Environ Sci Technol 39:4198-4205 (Pubitemid 40770250)
34. Runnegar MT, Kong SM, Zhong YZ, Ge JL, Lu SC (1994) The role of glutathione in the toxicity of a novel cyanobacterial alkaloid cylindrospermopsin in cultured rat hepatocytes. Biochem Biophys Res Commun 201:235-241 (Pubitemid 24213719)
35. SakerML, Thomas AD, Norton JH (1999) Cattlemortality attributed to the toxic cyanobacterium Cylindrospermopsis raciborskii in an outback region of the North Queensland. Environ Toxicol 14(1):179-182
36. Saker ML, Nogueira ICG, Vasconcelos VM, Neilan BA, Eaglesham GK, Pereira P (2003) First report and toxicological assessment of the cyanobacterium Cylindrospermopsis raciborskii from Portuguese freshwaters. Ecotox Environ Safe 55:243-250 (Pubitemid 36555411)
37. Saker ML, Vale M, Kramer D, Vasconcelos VM (2006) Molecular techniques for the early warning of toxic cyanobacteria blooms in freshwater lakes and rivers. Appl Microbiol Biotechnol 75 (2):441-449 (Pubitemid 46866520)
38. Schembri MA, Neilan BA, Saint CP (2001) Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environ Toxicol 16:413-421 (Pubitemid 33040532)
39. 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 (Farlowex Gomont) Speziale and Dyck. Harmful Algae 6:73-80. (Pubitemid 46038239)
40. Dyck. Harmful Algae 6:73-80Spoof L, Berg KA, Rapala J, Lahti K, Lepistö L, Metcalf JS, Codd GA, Meriluoto J (2006) First observation of cylindrospermopsin in Anabaena lapponica isolated from the boreal environment (Finland). Environ Toxicol 21:552-560 (Pubitemid 44788786)
41. Thomas AD, Saker ML, Norton JH, Olsen RD (1998) Cyanobacterium Cylindrospermopsis raciborskii as a probable cause of death in cattle in northern Queensland. Aust Vet J 76(9):592-594
42. Valério E, Pereira P, Saker ML, Franca S, Tenreiro R (2005) Molecular characterization of Cylindrospermopsis raciborskii strains isolated from Portuguese freshwaters. Harmful Algae 4:1044-1052 (Pubitemid 41562269)
43. Vasconcelos VM, Campos T, Amorim A, Soares AMVM (1993) Toxicidade de estirpes de cianobactérias isoladas a partir das lagoas das Braças, Vela e Mira. Boletim UCA, UCTRA, Univ Algarve 1:193-201
44. Welker M, Bickel H, Fastner J (2002) HPLC-PDA detection of cylindrospermopsin-opportunities and limits. Water Res 36:4659-4663
45. Wilson KM, Schembri MA, Baker PD, Saint CP (2000) Molecular characterization of the toxic cyanobacterium Cylindrospermopsis raciborskii and design of a species-specific PCR. Appl Environ Microbiol 66(1):332-338 (Pubitemid 30030536)
46. Yilmaz M, Philips ED, Szabo NJ, Badylak S (2008) A comparative study of Florida strains of Cylindrospermopsis and Aphanizomenon for cylindrospermopsin production. Toxicon 51:130-139