Use of a generalized additive model to investigate key abiotic factors affecting microcystin cellular quotas in heavy bloom areas of lake Taihu

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Tao, Min ^a   Xie, Ping ^a   Chen, Jun ^a   Qin, Boqiang ^b   Zhang, Dawen ^a   Niu, Yuan ^a   Zhang, Meng ^a   Wang, Qing ^a   Wu, Laiyan ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b NANJING INSTITUTE OF GEOGRAPHY AND LIMNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; DISSOLVED INORGANIC CARBON; MICROCYSTIN; UNCLASSIFIED DRUG; DRINKING WATER; FRESH WATER; OXYGEN;

ARTICLE; BACTERIAL OVERGROWTH; CARBON FIXATION; CHINA; CONCENTRATION (PARAMETERS); CONDUCTANCE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; GENERALIZED ADDITIVE MODEL; HEALTH HAZARD; LAKE; MICROCYSTIS; NONHUMAN; PH; POPULATION ABUNDANCE; STATISTICAL MODEL; WATER TEMPERATURE; CHEMISTRY; CYANOBACTERIUM; ENVIRONMENTAL MONITORING; GEOGRAPHY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SEASON; TEMPERATURE; WATER POLLUTION;

CYANOBACTERIA; MICROCYSTIS;

CHINA; CYANOBACTERIA; DRINKING WATER; ENVIRONMENTAL MONITORING; FRESH WATER; GEOGRAPHY; HYDROGEN-ION CONCENTRATION; LAKES; MICROCYSTINS; MICROCYSTIS; OXYGEN; SEASONS; TEMPERATURE; WATER MICROBIOLOGY; WATER POLLUTION;

EID: 84863165937     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032020     Document Type: Article

References (73)

1. Paerl HW, Fulton RS III, Moisander PH, Dyble J, (2001) Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Scientific World Journal 1: 76-113.
2. Havens KE, James T, East TL, Smith VH, (2003) N:P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution. Environmental Pollution 122: 379-390.
3. Te SH, Gin KYH, (2011) The dynamics of cyanobacteria and microcystin production in a tropical reservoir of Singapore. Harmful Algae 10: 319-329.
4. Carmichael WW, (1992) Cyanobacteria secondary metabolites-the cyanotoxins. Journal of Applied Bacteriology 72: 445-459.
5. Nishiwaki-Matsushima R, Ohta T, Nishiwaki S, (1992) Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. Journal of Cancer Research and Clinical Oncology 118: 420-424.
6. Gérard C, Poullain V, Lance E, Acou A, Brient L, et al. (2009) Influence of toxic cyanobacteria on community structure and microcystin accumulation of freshwater mollusks. Environmental Pollution 157: 609-617.
7. Lance E, Neffling MR, Gérard C, Meriluoto J, Bormans M, (2010) Accumulation of free and covalently bound microcystins in tissues of Lymnaea stagnalis (Gastropoda) following toxic cyanobacteria or dissolved microcystin-LR exposure. Environmental Pollution 158: 674-680.
8. Carmichael WW, (2001) Health effects of toxin-producing cyanobacteria: "the CyanoHABs". Human and Ecological Risk Assessment 7: 1393-1407.
9. Chen J, Zhang DW, Xie P, Wang Q, Ma ZM, (2009) Simultaneous determination of microcystin contaminations in various vertebrates (fish, turtle, duck and water bird) from a large eutrophic Chinese lake, Lake Taihu, with toxic Microcystis blooms. Science of the Total Environment 407: 3317-3322.
10. Chen JZ, Ye JY, Zhang HY, Jiang XJ, Zhang YX, et al. (2011) Freshwater toxic cyanobacteria induced DNA damage in apple (Malus pumila), rape (Brassica napus) and rice (Oryza sativa). Journal of Hazardous Materials 190: 240-244.
11. Jiang JL, Gu XY, Song R, Wang XR, Yang LY, (2011) Microcystin-LR induced oxidative stress and ultrastructural alterations in mesophyll cells of submerged macrophyte Vallisneria natans (Lour.) Hara. Journal of Hazardous Materials 190: 188-196.
12. Azevedo SMFO, Carmichael WW, Jochimsen EM, Rinehart KL, Lau S, et al. (2002) Human intoxication by microcystins during renal dialysis treatment in Caruaru-Brazil. Toxicology 181: 441-446.
13. Chen J, Xie P, Li L, Xu J, (2009) First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage. Toxicological Sciences 108: 81-89.
14. Orr PT, Jones GJ, (1998) Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnology and Oceanography 43: 1604-1614.
15. Halstvedt CB, Rohrlack T, Ptacnik R, Edvardsen B, (2008) On the effect of abiotic environmental factors on production of bioactive oligopeptides in field populations of Planktothrix spp. (Cyanobacteria). Journal of Plankton Research 30: 607-617.
16. Watanabe MF, Oishi S, (1985) Effect of environmental factors on toxicity of a cyanobacterium (Microcystis aeruginosa) under culture conditions. Applied and Environmental Microbiology 49: 1342-1344.
17. Sivonen K, (1990) Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains. Applied and Environmental Microbiology 56: 2658-2666.
18. 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 microcystins concentrations. Microbial Ecology 43: 443-454.
19. Dai RH, Liu HJ, Qu JH, Zhao X, Hou YN, (2009) Effects of amino acids on microcystin production of the Microcystis aeruginosa. Journal of Hazardous Materials 161: 730-736.
20. Wiedner C, Visser PM, Fastner J, Metcalf JS, Codd GA, et al. (2003) Effects of light on the microcystin content of Microcystis strain PCC 7806. Applied and Environmental Microbiology 69: 1475-1481.
21. Song LR, Sano T, Li RH, Watanabe M, Liu YD, et al. (1998) Microcystin production of Microcystis viridis (cyanobacteria) under different culture conditions. Phycological Research 46 (Suppl. 2): 19-23.
22. Jähnichen S, Petzoldt T, Benndorf J, (2001) Evidence for control of microcystin dynamics in Bautzen reservoir (Germany) by cyanobacterial population growth rates and dissolved inorganic carbon. Archiv fuer Hydrobiologie 150: 177-196.
23. Utkilen H, Gjølme N, (1995) Iron-stimulated toxin production in Microcystis aeruginosa. Applied and Environmental Microbiology 61: 797-800.
24. Wang JX, Xie P, Guo N, (2007) Effects of nonylphenol on the growthand microcystin production of Microcystis strains. Environmental Research 103: 70-78.
25. Jang MH, Ha K, Lucas MC, Joo GJ, Takamura N, (2004) Changes in microcystin production by Microcystis aeruginosa exposed to phytoplanktivorous and omnivorous fish. Aquatic Toxicology 68: 51-59.
26. Yang H, Xie P, Ke ZX, Liu YQ, Wu SK, et al. (2006) The impact of planktivorous fishes on microcystin concentrations in Meiliang Bay, Lake Taihu. China. J Freshw Ecol 21: 721-723.
27. Jang MH, Ha K, Takamura N, (2008) Microcystin production by Microcystis aeruginosa exposed to different stages of herbivorous zooplankton. Toxicon 51: 882-889.
28. Hastie TJ, Tibshirani RJ, (1990) Generalized Additive Models. Chapman and Hall, London, UK.
29. Yee TW, Mitchell ND, (1991) Generalized additive models in plant ecology. Journal of Vegetation Science 2: 587-602.
30. Pope CA III, Rodermund DL, Gee MM, (2007) Mortality Effects of a Copper Smelter Strike and Reduced Ambient Sulfate articulate Matter Air Pollution. Environmental Health Perspectives 115: 679-683.
31. Xie P, (2008) Historical Development of Cyanobacteria with Bloom Disaster in Lake Taihu, Science Press, Beijing, PRC (in Chinese).
32. Ma RH, Kong FX, Duan HT, Zhang SX, Kong WJ, et al. (2008) Spatio-temporal distribution of cyanobacteria blooms based on satellite imageries in Lake Taihu, China. Journal of Lake Science 20: 687-694 (in Chinese).
33. Shen PP, Shi Q, Hua ZC, Kong FX, Wang ZG, et al. (2003) Analysis of microcystins in cyanobacteria blooms and surface water samples from Meiliang Bay, Taihu Lake, China. Environment International 29: 641-647.
34. Liu YQ, Xie P, Zhang DW, Wen ZR, (2008) Seasonal dynamics of microcystins with associated biotic and abiotic parameters in two bays of Lake Taihu, the third largest freshwater lake in China. Bulletin of Environment Contamination and Toxicology 80: 24-29.
35. Ye WJ, Liu XL, Tan J, Li DT, Yang H, (2009) Diversity and dynamics of microcystin-Producing cyanobacteria in China's third largest lake, Lake Taihu. Harmful Algae 8: 637-644.
36. Wang Q, Niu YA, Xie P, Chen J, Ma ZM, et al. (2010) Factors affecting temporal and spatial variations of microcystins in Gonghu Bay of Lake Taihu, with potential risk of microcystin contamination to human health. Scientific World Journal 10: 1795-1809.
37. Wilhelm SW, Farnsley SE, LeCleir GR, Layton AC, Satchwell MF, et al. (2011) The relationships between nutrients, cyanobacterial toxins and the microbial community in Taihu (Lake Tai), China. Harmful Algae pp. 207-215.
38. Niu Y, Shen H, Chen J, Xie P, Yang X, et al. (2011) Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu, China. Water Res 45: 4169-4182.
39. Greenberg AE, Clesceri LS, Eaton AD, (1992) Standard methods for the examination of water and wastewater. American Public Health Association, Washington, D.C.
40. Parsons TR, Maita Y, Lalli CM, (1984) A Manual of Chemical and Biological Methods for Sea Water Analysis. Pergamon, Elmsford, New York, USA.
41. Hu HJ, Wei YX, (2006) Freshwater Algae in China, Science Press, Beijing, PRC (in Chinese).
42. John DM, Whitton BA, Brook AJ, (2002) The freshwater algal flora of the British Isles-an identification guide to freshwater and terrestrial algae. Cambridge University Press, UK.
43. SAS Institute Inc (1999) SAS Procedures Guide, Version 8 Cary, NC SAS Institute Inc.
44. Dong X, (2001) Fitting Generalized Additive Models with the GAM Procedure. SUGI Proceedings.
45. SAS Institute Inc (2004) SAS/STAT 9.1 User's Guide Cary, NC SAS Institute Inc.
46. Kurmayer R, Christiansen G, Chorus I, (2003) The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in Lake Wannsee. Appl Environmental Microbiology 69: 787-795.
47. Sabart M, Pobel D, Briand E, Combourieu B, Salençon MJ, et al. (2010) Spatiotemporal Variations in Microcystin Concentrations and in the Proportions of Microcystin-Producing Cells in Several Microcystis aeruginosa Populations. Applied and Environmental Microbiology 76: 4750-4759.
48. Joung SH, Oh HM, Ko SR, Ahn CY, (2011) Correlations between environmental factors and toxic and non-toxic Microcystis dynamics during bloom in Daechung Reservoir, Korea. Harmful Algae 10: 188-193.
49. Xu Y, Wu ZX, Yu BS, Peng XG, Yu LZ, et al. (2008) Non-microcystin producing Microcystis wesenbergii (Komárek) Komárek (Cyanobacteria) representing a main waterbloom-forming species in Chinese waters. Environmental Pollution 156: 162-167.
50. Dittmann E, Neilan BA, Erhard M, von Döhren H, Börner T, (1997) Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Mol Microbiol 26: 779-787.
51. Tillett D, Dittmann E, Erhard M, von Döhren H, Börner T, et al. (2000) Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chemistry & Biology 7: 753-64.
52. Furukawa N, Noda S, Tsuneda T, (2006) Highly sensitive real-time PCR assay for quantification of toxic cyanobacteria based on microcystin synthetase A gene. Journal of Bioscience and Bioengineering 102: 90-96.
53. Shi LM, Cai YF, Yang HL, Li PF, Kong FX, et al. (2009) Dynamics of composition of different Microcystis spp. genotypes and abundance of toxic Microcystis in Meiliang Bay of Lake Taihu during bloom. Journal of Lake Science 21: 801-805 (in Chinese).
54. Kotak BG, Lam AKY, Prepas EE, (1995) Variability of hepatotoxin microcystin-LR in hypereutrophic drinking water lakes. Journal of Phycology 31: 248-263.
55. 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. Canadian Journal of Fisheries and Aquatic Sciences 57: 1584-1593.
56. Haney JF, Ikawa M, (2000) Final Report: A Survey of 50 NH Lakes for Microcystins (MCs), Report 65. New Hampshire Water Resources Research Center, Durham.
57. Ozawa K, Fujioka H, Muranaka M, Yokoyama A, Katagami Y, et al. (2005) Spatial distribution and temporal variation of Microcystis concentration in Lake Biwa. Environmental Toxicology 20: 270-276.
58. Zhang DW, Xie P, Liu YQ, Chen J, Wen ZR, (2009) Spatial and temporal variations of microcystins in hepatopancreas of a freshwater snail from Lake Taihu. Ecotoxicology and Environmental Safety 72: 466-472.
59. Casanova MT, Burch MD, Brock MA, Bond PM, (1999) Does toxic Microcystis aeruginosa affect aquatic plant establishment? Environmental Toxicology 14: 97-109.
60. LeBlanc S, Pick FR, Aranda-Rodriguez R, (2005) Allelopathic effects of the toxic cyanobacterium Microcystis aeruginosa on duckweed, Lemna gibba L. Environmental Toxicology 20: 67-73.
61. Zhang M, Wang ZQ, Xu J, Liu YQ, Ni LY, et al. (2010) Ammonium, microcystins, and hypoxia of blooms in eutrophic water cause oxidative stress and C-N imbalance in submersed and floating-leaved aquatic plants in Lake Taihu, China. Chemosphere 82: 329-339.
62. Zhu JY, Liu BY, Wang J, Gao YN, Wu ZB, (2010) Study on the mechanism of allelopathic influence on cyanobacteria and chlorophytes by submerged macrophyte (Myriophyllum spicatum) and its secretion. Aquatic Toxicology 98: 196-203.
63. Yoshida M, Yoshida T, Takashima Y, Hosoda N, Hiroishi S, (2007) Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microbiol Lett 266: 49-53.
64. Davis TW, Berry DL, Boyer GL, Gobler CJ, (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.
65. Kaebernick M, Neilan BA, Börner T, Dittmann E, (2000) Light and the transcriptional response of the microcystin biosynthesis gene cluster. Appl Environ Microbiol 66: 3387-3392.
66. Sevilla E, Martin-Luna B, Vela L, Bes MT, Fillat MF, et al. (2008) Iron availability affects mcyD expression and microcystin-LR synthesis in Microcystis aeruginosa PCC7806. Environmental Microbiology 10: 2476-2483.
67. Janse I, Kardinaal WEA, Meima M, Fastner J, Visser PM, et al. (2004) Toxic and nontoxic Microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity. Applied and Environmental Microbiology 70: 3979-3987.
68. Giordano M, Beardall J, Raven JA, (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 56: 99-131.
69. Kaplan A, Schwarz R, Lieman-Hurwitz J, Reinhold L, (1991) Physiological and molecular aspects of the inorganic carbon-concentrating mechanism in cyanobacteria. Plant Physiol 97: 851-855.
70. Miller AG, Turpin DH, Canvin DT, (1984) Na+ requirement for growth, photosynthesis, and pH regulation in the alkalotolerant cyanobacterium Synechococcus leopoliensis. Journal of Bacteriology 159: 100-106.
71. Jähnichen S, Ihle T, Petzoldt T, Benndorf J, (2007) Impact of inorganic carbon availability on microcystin production by Microcystis aeruginosa PCC 7806. Applied and Environmental Microbiology 73: 6994-7002.
72. Van der Westhuizen AJ, Eloff JN, (1985) Effects of temperature and light on the toxicity and growth of the blue-green alga Microcystis aeguginosa (UV-006). Planta 163: 55-59.
73. Li SX, Xie P, Xu J, Zhang X, Qin J, et al. (2007) Factors shaping the pattern of seasonal variations of microcystins in Lake Xingyun, a subtropical plateau lake in China. Bulletin of Environment Contamination and Toxicology 78: 226-230.