Sampling and analysis of microcystins: Implications for the development of standardized methods

Environmental Toxicology

Volumn 22, Issue 2, 2007, Pages 132-143

  Tillmanns, Angeline R ^a   Pick, Frances R ^a   Aranda Rodriguez, Rocio ^b  

^a UNIVERSITY OF OTTAWA   (Canada)

^b HEALTH CANADA   (Canada)

Author keywords

Cyanobacteria; ELISA; HPLC; Lake sampling; Microcystins

Indexed keywords

ABSORPTION; BACTERIA; LAKES; MATHEMATICAL MODELS; SAMPLING; ULTRAVIOLET RADIATION;

HIGHER CONCENTRATIONS; LAKE SAMPLING; MICROCYSTINS (MC); PLANKTONS;

AMINO ACIDS;

CHLOROPHYLL A; CYANOGINOSIN; CYANOGINOSIN LR; FRESH WATER; LAKE WATER; SURFACE WATER;

CHEMICAL ANALYSIS; CYANOBACTERIUM; IMMUNOASSAY; LACUSTRINE ENVIRONMENT; LIQUID CHROMATOGRAPHY; SAMPLING BIAS; TOXIN; WATER QUALITY;

ALGAL BLOOM; ARTICLE; CHEMICAL ANALYSIS; CYANOBACTERIUM; ENZYME LINKED IMMUNOSORBENT ASSAY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIGHT ABSORPTION; MEASUREMENT; PHOTOCHEMISTRY; PHOTODIODE ARRAY; PLANKTON COUNTER; PRIORITY JOURNAL; STANDARD; TOXICOLOGICAL PARAMETERS; TOXIN ANALYSIS; WATER SAMPLING;

ALGAE, GREEN; BACTERIAL TOXINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DIATOMS; ENVIRONMENTAL MONITORING; ENZYME-LINKED IMMUNOSORBENT ASSAY; FRESH WATER; MARINE TOXINS; MICROCYSTINS; WATER POLLUTANTS;

CYANOBACTERIA;

EID: 34047159451     PISSN: 15204081     EISSN: 15227278     Source Type: Journal    
DOI: 10.1002/tox.20250     Document Type: Article

References (87)

1. Albay M, Akcaalan R, Tufekci H, Metcalf JS, Beattie KA, Codd GA. 2003. Depth profiles of cyanobacterial hepatotoxins (microcystins) in three Turkish freshwater lakes. Hydrobiologia 505:89-95.
2. Amé MV, del Pilar Díaz M, Wunderlin DA. 2003. Occurrence of toxic cyanobacterial blooms in San Roque Reservoir (Córdoba, Argentina): A field and chemometric study. Environ Toxicol 18:192-201.
3. An J, Carmichael WW. 1994. Use of a colorimetric protein phosphatase inhibition assay and enzyme linked immunosorbent assay for the study of microcystins and nodularins. Toxicon 32:1495-1507.
4. Aranda-Rodriguez R, Tillmanns A, Benoit F, Pick FR, Harvie J, Solenaia L. 2005. Pressurized liquid extraction of toxins from cyanobacterial cells. Environ Toxicol 20:390-396.
5. Baldia SF, Conaco MCG, Nishijima T, Imanishi S, Harada K. 2003. Microcystin production during algal bloom occurrence in Laguna de Bay, the Philippines. Fisheries Science. 69:110-116.
6. Ballot A, Pflugmacher S, Wiegand C, Kotut K, Krienitz L. 2003. Cyanobacterial toxins in Lake Baringo, Kenya. Limnologica 33: 2-9.
7. Ballot A, Krienitz L, Kotut K, Wiegand C, Metcalf JS, Codd GA, Pflugmacher S. 2004. Cyanobacteria and cyanobacterial toxins in three alkaline Rift Valley lakes of Kenya-Lakes Bogoria Nakura and Elmenteita. J Plankton Res 26:925-935.
8. Ballot A, Krienitz L, Kotut K, Wiegand C, Pflugmacher S. 2005. Cyanobacteria and cyanobacterial toxins in the alkaline crater lakes Sonachi and Simbi, Kenya. Harmful Algae 4:139-150.
9. Billam M, Tang L, Cai Q, Mukhi S, Guan H, Wang P, Wang Z, Theodorakis CW, Kendall RJ, Wang J. 2006. Seasonal varia in the concentration of microcystin-LR in two lakes in western Texas, USA. Environ Toxicol Chem 25:349-355.
10. Bogialli S, Bruno M, Curini R, Di Corcia A, Fanali C, Laganà A. 2006. Monitoring algal toxins in lake water by liquid chromotography tandem mass spectrometry. Environ Sci Technol 40: 2917-2923.
11. Briand JF, Robillot C, Quiblier-Llobéras C, Bernard C. 2002. A perennial bloom of Planktothrix agardhii (Cyanobacteria) in a shallow eutrophic French lake: Limnological and microcystin production studies. Arch Hydrobiol 153:605-622.
12. Briand JF, Jacquet S, Flinois C, Avois-Jacquet C, Maisonnette C, Leberre B, Humbert JF. 2005. Variations in the microcystin production of Planktothrix rubescens (Cyanobacteria) assessed from a four-year survey of Lac du Bourget (France) and from Laboratory Experiments. Microb Ecol 50:418-428.
13. Burnison BK. 1980. Modified dimethysulfoxide (DMSO) extraction from chlorophyll analysis of phytoplankton. Can J Fish Aquat Sci 37:729-733.
14. Carmichael WW. 2001. Health effects of toxin-producing cyanobacteria: "The CyanoHABs". Hum Ecol Risk Assess 7:1393-1407.
15. Codd GA. 2000. Cyanobacterial toxins, the perception of water quality, and the prioritization of eutrophication control. Ecol Eng 16:51-60.
16. Conti ALR, Guerrero JM, Regueira JM. 2006. Levels of microcystins in two Argentinean reservoirs used for water supply and recreation: Differences in implementation of safe levels. Environ Toxicol 20:263-269.
17. Cuvin-Aralar ML, Fastner J, Focken U, Becker K, Aralar EV. 2002. Microcystins in natural blooms and laboratory cultured Microcystis aeruginosa from Laguna de Bay, Philippines. Syst Appl Microbiol 25:179-182.
18. Domingos P, Rubim TK, Molica RJR, Azevedo SMFO, Carmichael WW. 1999. First report of microcystin production by picoplanktonic cyanobacteria isolated from a northeast Brazilian drinking water supply. Environ Toxicol 14:31-35.
19. Downing JA, Watson SB, McCauley E. 2001. Predicting cyanobacteria dominance in lakes. Can J Fish Aquat Sci 58:1905-1908.
20. Fastner J, Codd GA, Metcalf JS, Woitke P, Wiedner C, Utkilen H. 2002. An international intercomparison exercise for the determination of purified microcystin-LR and microcystins in cyanobacterial field material. Anal Bioanal Chem 374:437-444.
21. Fischer WJ, Garthwaite I, Miles CO, Ross KM, Aggen JB, Chamberlin AR, Towers NR, Dietrich DR. 2001. Congener-independent immunoassay for microcystins and nodularins. Environ Sci Technol 35:4849-4856.
22. Frank CAP. 2002. Microcystin-producing cyanobacteria in recreational waters in southwestern Germany. Environ Toxicol 17: 361-366.
23. George DG, Heaney SI. 1978. Factors influencing the spatial distribution of phytoplankton in a small productive lake. J Ecol 66:133-155.
24. Giani A, Bird DF, Prairie YT, Lawrence JF. 2005. Empirical study of cyanobacterial toxicity along a trophic gradient of lakes. Can J Fish Aquat Sci 62:2100-2109.
25. Graham JL, Jones JR, Jones SB, Downing JA, Clevenger TE. 2004. Environmental factors influencing microcystin distribution and concentration in the Midwestern United States. Water Res 38:4395-4404.
26. Graham JL, Jones JR, Jones SB, Clevenger TE. 2006. Spatial and temporal dynamics of microcystin in a Missouri Reservoir. Lake Reservoir Manage 22:59-68.
27. Haider S, Naithani V, Viswanathan PN, Kakkar P. 2003. Cyanobacterial toxins: A growing environmental concern. Chemosphere 52:1-21.
28. 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.
29. Harada K, Murata H, Qiang Z, Suzuki M, Kondo F. 1996. Mass spectrometric screening method for microcystins in cyanobacteria. Toxicon 34:701-710.
30. Harada K, Kondo F, Lawton LA. 1999. Laboratory analysis of cyanotoxins. In: Chorus I, Bartram J, editors. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management. WHO. pp 370-399.
31. Harris DC. 2003. Quantitative Chemical Analysis. Freeman, Basingstoke, Macmillan, New York. 744 p.
32. Health Canada. Guidelines for Canadian drinking water quality: Supporting documentation-Cyanobacterial toxins-microcystin-LR. 1-15. 2002. Ottawa, ON, Water Quality and Health Bureau, Healthy Environments and Consumer Safety Branch, Health Canada.
33. Hotto A, Satchwell M, Boyer G. 2005. Seasonal production and molecular characterization of microcystins in Oneida Lake, New York, USA. Environ Toxicol 20:243-248.
34. Hummert Ch, Dahlmann J, Reinhardt K, Dang HPhH, Dang DK, Luckas B. 2001. Liquid chromatography-Mass spectrometry identification of microcystins in Microcystis aeruginosa strain from Lake Thanh Cong, Hanoi, Vietnam. Chromatographia 54: 569-575.
35. ISO. 2005. Water quality-Determination of microcystins-Method using solid phase extraction (SPE) and high performance liquid chromotography (HPLC) with ultraviolet (UV) detection. 1-17. International Organization for Standardization.
36. Jann-Para G, Schwob I, Feuillade J. 2004. Occurrence of toxic Planktothrix rubescens blooms in lake Nantua, France. Toxicon 43:279-285.
37. Janse I, Kardinaal WEA, Agterveld MK, Meima M, Visser PM, Zwart G. 2005. Contrasting microcystin production and cyanobacterial population dynamics in two Planktothrix dominated freshwater lakes. Environ Microb 7:1514-1524.
38. Jayatissa LP, Silva EIL, McElhiney J, Lawton LA. 2006. Occurrence of toxigenic cyanobacterial blooms in freshwaters of Sri Lanka. Syst Appl Microbiol 29:156-164.
39. Jeffrey SW, Humphrey GF. 1975. New spectrophotometric equations for determining chlorophyll a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen 167:191-194.
40. Johnston BR, Jacoby JM. 2003. Cyanobacterial toxicity and migration in a mesotrophic lake in western Washington, USA. Hydrobiologia 495:79-91.
41. Jones SB, Jones JR. 2002. Seasonal variation in cyanobacterial toxin production in two Nepalese lakes. Verh Internat Verein Limnol 28:1017-1022.
42. Jurczak T, Tarczyñska M, Karlsson K, Meriluoto J. 2004. Characterization and diversity of cyanobacterial hepatotoxins (microcystins) in blooms from Polish freshwater identified by liquid chromatography-electrospray ionization mass spectrometry. Chromatographia 59:571-578.
43. Kemp A, John J. 2006. Microcystins associated with Microcystis dominated blooms in the southwest wetlands, Western Australia. Environ Toxicol 21:125-130.
44. Kotak BG, Zurawell RW, Prepas EE, Holmes CFB. 1996. Microcystin-LR concentrations in aquatic food web compartments from lakes of varying trophic status. Can J Fish Aquat Sci 53: 1974-1985.
45. Kotak BG, Lam AKY, Prepas EE, Hrudey SE. 2000. Role of chemical and physical variables in regulating microcystin-LR concentration in phytoplankton of eutrophic lakes. Can J Fish Aquat Sci 57:1584-1593.
46. Kubwabo C, Vais N, Benoit FM. 2004. Identification of microcystin-RR and [Dha7] microcystin-RR in commercial standards by electrospray ionization mass spectrometry. J AOAC Int 87: 1028-1031.
47. Kurmayer R, Christiansen G, Chorus I. 2003. The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystin sp. and determines its microcystin net production in Lake Wansee. Appl Environ Microbiol 69:787-795.
48. Lathrop RC. 1999. Summer water clarity responses to phosphorus. Daphnia grazing, and internal mixing in Lake Mendota. Limnol Oceanogr 44:137-146.
49. Lawton LA, Edwards C, Codd GA. 1994. Extraction and high-performance liquid Chromatographic method for the determination of microcystins in raw and treated waters. Analyst 119:1525-1530.
50. Lindholm T, Vesterkvist P, Spoof L, Lundberg-Niinisto C, Meriluoto J. 2003. Microcystin occurrence in lakes in Aland, SW Finland. Hydrobiologia 505:129-138.
51. Maatouk I, Bouaïcha N, Fontan D, Levi Y. 2002. Seasonal variation of microcystin concentrations in the Saint-Caprais reservoir (France) and their removal in a small full-scale treatment plant. Water Res 36:2891-2897.
52. Mankiewicz J, Komárková J, Izydorczyk K, Jurczak T, Tarczynska M, Zalewski M. 2005. Hepatotoxic cyanobacterial blooms in the lakes of Nothern Poland. Environ Toxicol 20:499-506.
53. Mathys W, Surhold B. 2004. Analysis of microcystins in freshwater samples using high performance liquid chromotography and an enzyme-linked immunosorbent assay. Int J Hyg Environ Health 207:601-605.
54. McElhiney J, Lawton LA. 2005. Detection of the cyanobacterial hepatotoxins microcystins. Toxicol Appl Pharmacol 203:219-230.
55. Metcalf JS, Hyenstrand P, Beattie KA, Codd GA. 2000. Effects of physiochemical variables and cyanobacterial extracts on the immunoassay of microcystin-LR by two ELISA kits. J Appl Microbiol 89:532-538.
56. Metcalf JS, Beattie KA, Ressler J, Gerbersdorf S, Pflugmacher S, Codd GA. 2002. Cross-reactivity and performance assessment of four microcystin immunoassays with detoxication products of the cyanobacterial toxin, microcystin-LR. J Water Res Tech-AQUA 51:145-151.
57. Metcalf JS, Codd GA. 2003. Analysis of cyanobacterial toxins by immunological methods. Chem Res Toxicol 16:1-8.
58. Moreno IM, Pereira P, Franca S, Camean A. 2004. Toxic cyanobacteria strains isolated from blooms in the Guadiana River (southwestern Spain). Biol Res 37:405-471.
59. Moreno I, Repetto G, Carballal E, Gago A, Camean AM. 2005. Cyanobacteria and microcystins occurrence in the Guadiana River (SW Spain). Int J Environ Anal Chem 85:461-474.
60. Mountfort DO, Holland P, Sprosen J. 2005. Method of detecting classes of microcystins by combination of protein phosphatase inhibition assay and ELISA: Comparison with LC-MS. Toxicon 45:199-206.
61. Msagati TAM, Siame BA, Shushu DD. 2006. Evaluation of methods for the isolation, detection and quantification of cyanobacterial hepatotoxins. Aquat Toxicol 78:382-397.
62. Murphy TP, Irvine K, Guo J, Davies J, Murkin H, Charlton M, Watson SB. 2003. New microcystin concerns in the lower Great Lakes. Water Qual Res J Can 38:127-140.
63. Nasri A, Bouaicha N, Fastner J. 2004. First report of a microcystin-containing bloom of cyanobacteria Microcystis spp. in Lake Oubeira, Eastern Algeria. Arch Environ Contam Toxicol 46: 197-202.
64. National Health and Medical Research Council. Australian Drinking Water Guidelines. 1-376. 1996. Agriculture and Resource Management Council of Australia and New Zealand.
65. Ozawa K, Fujioka H, Muranaka M, Yokoyama A, Katagami Y, Homma T, Ishikawa K, Tsujimura S, Kumagai M, Watanabe MF Park H. 2005. Spatial distribution and temporal variation of Microcystis species composition and microcystin concentration in Lake Biwa. Environ Toxicol 20:270-276.
66. Padilla C, Sanz-Alférez S, del Campo FF. 2006. Toxin characterization and identification of a Microcystis flos-aquae strain from a Spanish drinking-water reservoir. Arch Hydrobiol 165:383-399.
67. Reynolds CS, Wiseman SW, Clarke MJO. 1984. Growth and loss rate responses of phytoplankton to intermittent artificial mixing and their potential application to the control of planktonic algal biomass. J Appl Ecol 21:11-39.
68. Rinehart KL, Namikoshi M, Choi BW. 1994. Structure and biosynthesis of toxins from blue-green algae (cyanobacteria). J Appl Phycol 6:159-176.
69. Rolland A, Bird DF, Giani A. 2005. Seasonal changes in composition of the cyanobacterial community and the occurrence of hepatotoxic blooms in the eastern townships, Quebec, Canada. J Plankton Res 27:683-694.
70. Sabour B, Loudiki M, Oudra B, Vasconcelos V, Martins R, Oubraim S, Fawzi B. 2002. Toxicology of a Microcystis ichthyoblabe waterbloom from Lake Oued Mellah (Morocco). Environ Toxicol 17:24-31.
71. Scott WE. 1991. Occurrence and significance of toxic cyanobacteria in Southern Africa. Water Sci Technol 23:175-180.
72. Sekadende BC, Lyimo TJ, Kurmayer R. 2005. Microcystin production by cyanobacteria in the Mwanza Gulf (Lake Victoria, Tanzania). Hydrobiologia 543:299-304.
73. Shen PP, Shi Q, Hua ZC, Kong FX, Wang ZG, Zhuang SX, Chen DC. 2003. Analysis of microcystins in cyanobacteria blooms and surface water samples from Meiliang Bay, Taihu Lake, China. Environ Int 29:641-647.
74. Sivonen K, Jones G. 1999. Cyanobacterial toxins. In: Chorus I, Bartram J, editors. Toxic Cyanobacteria in Water-A Guide to Their Public Health Consequences, Monitoring and Management. E & FN Spoon, London, pp 41-111.
75. Thostrup L, Christoffersen K. 1999. Accumulation of microcystin in Daphnia magma feeding on toxic Microcystis. Arch Hydrobiol 145:447-467.
76. Utkilen H, Fastner J, Bartram J. 1999. Fieldwork: site inspection and sampling. In: Chorus I, Bartram J, editors. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management. World Health Organization, pp 1-17.
77. Vieira JMS, Azevedo MTP, Azevedo SMFO, Honda RY, Correa B. 2005. Toxic cyanobacteria and microcystin concentrations in a public water supply reservoir in the Brazilian Amazonian region. Toxicon 45:901-909.
78. Wang X, Parkpian P, Fujimoto N, Ruchirawat KM, DeLaune RD, Jugsujinda A. 2002. Environmental conditions associating microcystins production to Microcystis aeruginosa in a reservoir of Thailand. J Environ Sci Health A 37:1181-1207.
79. Watanabe MM, Kaya K, Takamura N. 1992. Fate of the toxic cyclic heptapeptides, the microcystins, from blooms of Microcystis (Cyanobacteria) in a hypertrophic lake. J Phycol 28:761-767.
80. Welker M, von Dohren H, Tauscher H, Steinberg CEW, Erhard M. 2003. Toxic Microcystis in shallow lake Muggelsee (Germany)-Dynamics, distribution, diversity. Arch Hydrobiol 157:227-248.
81. Wetzel RG, Likens GE. 1990. Limnological Analysis. New York: Springer-Verlag. 391 p.
82. White SA, Fabbro LD, Duivenvoorden LJ. 2003. Changes in cyanoprokaryote populations. Microcystis morphology, and microcystin concentrations in Lake Elphinstone (Central Queensland, Australia). Environ Toxicol 18:403-412.
83. Willame R, Jurczak T, Iffly J, Kull T, Meriluoto J, Hoffmann L. 2005. Distribution of hepatotoxic cyanobacterial blooms in Belgium and Luxembourg. Hydrobiologia 551:99-117.
84. Wirsing B, Flury T, Wiedner C, Neumann U, Weckesser J. 1999. Estimation of the microcystin content in cyanobacterial field samples from German Lakes using the colorimetric protein-phosphatase inhibition assay and RP-HPLC. Environ Toxicol 14:23-29.
85. World Health Organization. 2004. Guidelines for Drinking Water Quality, 3rd edition, Geneva: WHO, Volume I. 540 p.
86. Zar JH. 1999. Biostatistical Analysis. Upper Saddle River, New Jersey: Prentice-Hall. 670 p.
87. Znachor P, Jurczak T, Komarkova J, Jezberova J, Mankiewicz J, Kastovska K, Zapomelova E. 2006. Summer changes in cyanobacterial bloom composition and microcystin concentration in eutrophic Czech reservoirs. Environ Toxicol 21:236-243.