Multi-year assessment of toxic genotypes and microcystin concentration in northern lake taihu, China

Toxins

Volumn 8, Issue 1, 2016, Pages

  Hu, Lili ^a,b   Shan, Kun ^c   Lin, Lizhou ^a,b   Shen, Wei ^d   Huang, Licheng ^a,b   Gan, Nanqin ^a   Song, Lirong ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c University of Chinese Academy of Sciences   (China)

^d Changzhou Environmental Monitoring Center   (China)

Author keywords

Lake taihu; Microcystins; Microcystis morphospecies; Nitrogen; QPCR

Indexed keywords

AMMONIA; CHLOROPHYLL A; DNA 16S; MICROCYSTIN; NITRATE; NITROGEN; BACTERIAL DNA; RIBOSOME DNA; WATER POLLUTANT;

ALGAL BLOOM; APHANIZOMENON; ARTICLE; CHINA; DNA EXTRACTION; DRY WEIGHT; ENVIRONMENTAL FACTOR; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LAKE; MICROCYSTIS; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SEASONAL POPULATION DYNAMICS; TOXIC CONCENTRATION; ANALYSIS; ENVIRONMENTAL MONITORING; EUTROPHICATION; GENETICS; GENOTYPE; ISOLATION AND PURIFICATION; WATER POLLUTANT;

CHINA; DNA, BACTERIAL; DNA, RIBOSOMAL; ENVIRONMENTAL MONITORING; EUTROPHICATION; GENOTYPE; LAKES; MICROCYSTINS; MICROCYSTIS; WATER POLLUTANTS;

EID: 84954406800     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins8010023     Document Type: Article

References (55)

1. Falconer, I.R.; Humpage, A.R. Health risk assessment of cyanobacterial (blue-green algal) toxins in drinking water. Int. J. Environ. Res. Pubulic Health 2005, 2, 43-50. [CrossRef]
2. Codd, G.A.; Lindsay, J.; Young, F.M.; Morrison, L.F.; Metcalf, J.S. From mass mortalities to management measures. In Harmful Cyanobacteria; Huisman, J., Matthijs, H.C.P., Visser, P.M., Eds.; Springer Netherlands: Dordrecht, The Netherland, 2005; pp. 1-23.
3. Honkanen, R.E.; Zwiller, J.; Moore, R.E.; Daily, S.L.; Khatra, B.S.; Dukelow, M.; Boynton, A.L. Characterization of microcystin-LR, a potent inhibitor of type 1 and type 2A protein phosphatases. J. Biol. Chem. 1990, 265, 19401-19404. [PubMed]
4. Meiβner, K.; Dittmann, E.; Börner, T. Toxic and non-toxic strains of the cyanobacterium Microcystis aeruginosa contain sequences homologous to peptide synthetase genes. FEMS Microbiol. Lett. 1996, 135, 295-303. [CrossRef]
5. Dittmann, E.; Neilan, B.A.; Erhard, M.; Döhren, H.V.; Börner, T. Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Mol. Microbiol. 1997, 26, 779-787. [CrossRef] [PubMed]
6. Tillett, D.; Parker, D.L.; Neilan, B.A. Detection of toxigenicity by a probe for the microcystin synthetase a gene (mcyA) of the cyanobacterial genus Microcystis: Comparison of toxicities with 16S rRNA and phycocyanin operon (phycocyanin intergenic spacer) phylogenies. Appl. Environ. Microb. 2001, 67, 2810-2818. [CrossRef] [PubMed]
7. Mikalsen, B.; Boison, G.; Skulberg, O.M.; Fastner, J.; Davies,W.; Gabrielsen, T.M.; Rudi, K.; Jakobsen, K.S. Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains. J. Bacteriol. 2003, 185, 2774-2785. [CrossRef] [PubMed]
8. Welker, M.; von Döhren, H. Cyanobacterial peptides-nature's own combinatorial biosynthesis. FEMS Microbiol. Rev. 2006, 30, 530-563. [CrossRef] [PubMed]
9. Bortoli, S.; Oliveira-Silva, D.; Krüger, T.; Dörr, F.; Colepicolo, P.; Volmer, D.; Pinto, E. Growth and microcystin production of a Brazilian Microcystis aeruginosa strain (LTPNA 02) under different nutrient conditions. Rev. Bras. Farmacogn. 2014, 24, 389-398. [CrossRef]
10. Gupta, N.; Pant, S.C.; Vijayaraghavan, R.; Lakshmana Rao, P.V. Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin variants (LR, RR, YR) in mice. Toxicology 2003, 188, 285-296. [CrossRef]
11. Kurmayer, R.; Kutzenberger, T. Application of real-time PCR for quantification of microcystin genotypes in a population of the toxic cyanobacterium Microcystis sp. Appl. Environ. Microb. 2003, 69, 6723-6730. [CrossRef]
12. Rinta-Kanto, J.M.; Ouellette, A.; Boyer, G.L.; Twiss, M.R.; Bridgeman, T.B.;Wilhelm, S.W. Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in western Lake Erie using quantitative real-time PCR. Environ. Sci. Technol. 2005, 39, 4198-4205. [CrossRef] [PubMed]
13. Furukawa, K.; Noda, N.; Tsuneda, S.; Saito, T.; Itayama, T.; Inamori, Y. Highly sensitive real-time PCR assay for quantification of toxic cyanobacteria based on microcystin synthetase A gene. J. Biosci. Bioeng. 2006, 102, 90-96. [CrossRef] [PubMed]
14. Hotto, A.M.; Satchwell, M.F.; Berry, D.L.; Gobler, C.J.; Boyer, G.L. Spatial and temporal diversity of microcystins and microcystin-producing genotypes in Oneida Lake, NY. Harmful Algae 2008, 7, 671-681. [CrossRef]
15. Davis, T.W.; Berry, D.L.; Boyer, G.L.; Gobler, C.J. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 2009, 8, 715-725. [CrossRef]
16. Okello,W.; Portmann, C.; Erhard, M.; Gademann, K.; Kurmayer, R. Occurrence of microcystin-producing cyanobacteria in Ugandan freshwater habitats. Environ. Toxicol. 2010, 25, 367-380. [CrossRef] [PubMed]
17. Srivastava, A.; Choi, G.G.; Ahn, C.Y.; Oh, Hee-Mock.; Ravi, A.K.; Asthana, R.K. Dynamics of microcystin production and quantification of potentially toxigenic Microcystis sp. using real-time PCR.Water Res. 2012, 46, 817-827. [CrossRef] [PubMed]
18. Ye,W.; Liu, X.L.; Tan, J.; Li, D.; Yang, H. Diversity and dynamics of microcystin-Producing cyanobacteria in China's third largest lake, Lake Taihu. Harmful Algae 2009, 8, 637-644. [CrossRef]
19. Sabart, M.; Pobel, D.; Briand, E.; Combourieu, B.; Salencon, M.J.; Humbert, J.F.; Latour, D. Spatiotemporal variations in microcystin concentrations and in the proportions of microcystin-producing cells in several Microcystis aeruginosa populations. Appl. Environ. Microb. 2010, 76, 4750-4759. [CrossRef] [PubMed]
20. Guedes, I.A.; da Costa Leite, D.M.; Manhães, L.A.; Bisch, P.M.; Azevedo, S.; Pacheco, A. Fluctuations in microcystin concentrations, potentially toxic Microcystis and genotype diversity in a cyanobacterial community from a tropical reservoir. Harmful Algae 2014, 39, 303-309. [CrossRef]
21. Jacoby, J.; Collier, D.C.; Welch, E.B.; Hardy, F.J.; Crayto, M. Environmental factors associated with a toxic bloom of Microcystis aeruginosa. Can. J. Fish. Aquat. Sci. 2000, 57, 231-240. [CrossRef]
22. Kotak, B.G.; Lam, A.; Prepas, E.E.; Hrudey, S. Role of chemical and physical variables in regulating microcystin-LR concentration in phytoplankton of eutrophic lakes. Can. J. Fish. Aquat. Sci. 2000, 57, 1584-1593. [CrossRef]
23. Izydorczyk, K.; Jurczak, T.; Wojtal-Frankiewicz, A.; Skowron, A.; Mankiewicz-Boczek, J.; Tarczý nska, M. Influence of abiotic and biotic factors on microcystin content in Microcystis aeruginosa cells in a eutrophic temperate reservoir. J. Plankton Res. 2008, 30, 393-400. [CrossRef]
24. Horst, G.P.; Sarnelle, O.; White, J.D.; Hamilton, S.K.; Kaul, R.; Bressie, J.D. Nitrogen availability increases the toxin quota of a harmful cyanobacterium, Microcystis aeruginosa. Water Res. 2014, 54, 188-198. [CrossRef] [PubMed]
25. Park, H.D.; Kim, B.; Kim, E.; Okino, T. Hepatotoxic microcystins and neurotoxic anatoxin-a in cyanobacterial blooms from Korean lakes. Environ. Toxicol. Water Qual. 1998, 13, 225-234. [CrossRef]
26. Honma, T.; Park, H.D. Influences of nitrate and phosphate concentrations on Microcystis species composition and microcystin concentration in Lake Suwa. J. Jpn. Soc. Water Environ. 2005, 28, 373-378. [CrossRef]
27. Yamamoto, Y.; Nakahara, H. Seasonal variations in the morphology of bloom-forming cyanobacteria in a eutrophic pond. Limnology 2009, 10, 185-193. [CrossRef]
28. Kurmayer, R.; Dittmann, E.; Fastner, J.; Chorus, I. Diversity of microcystin genes within a population of the toxic cyanobacterium Microcystis spp. in lakeWannsee (Berlin, Germany). Microb. Ecol. 2002, 43, 107-118. [CrossRef] [PubMed]
29. Via-Ordorika, L.; Fastner, J.; Kurmayer, R.; Hisbergues, M.; Dittmann, E.; Komarek, J.; Erhard, M.; Chorus, I. Distribution of microcystin-producing and non-microcystin-producing Microcystis sp. in European freshwater bodies: Detection of microcystins and microcystin genes in individual colonies. Syst. Appl. Microbiol. 2004, 27, 592-602. [CrossRef] [PubMed]
30. Chen,W.; Peng, L.;Wan, N.; Song, L. Mechanism study on the frequent variations of cell-bound microcystins in cyanobacterial blooms in Lake Taihu: Implications for Water Quality Monitoring and Assessments. Chemosphere 2009, 77, 1585-1593. [CrossRef] [PubMed]
31. Kurmayer, R.; Christiansen, G.; Chorus, I. The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in Lake Wannsee. Appl. Environ. Microb. 2003, 69, 787-795. [CrossRef]
32. Wang, X.; Sun, M.; Xie, M.; Liu, M.; Luo, L.; Li, P.F.; Kong, F.X. Differences in microcystin production and genotype composition among Microcystis colonies of different sizes in Lake Taihu. Water Res. 2013, 47, 5659-5669. [CrossRef] [PubMed]
33. Qin, B.; Xu, P.; Wu, Q.; Luo, L.C.; Zhang, Y.L. Environmental issues of lake Taihu, China. Hydrobiologia 2007, 581, 3-14. [CrossRef]
34. Song, L.; Chen, W.; Peng, L.; Wan, N.; Gan, N.Q.; Zhang, X.M. Distribution and bioaccumulation of microcystins in water columns: A Systematic Investigation into the Environmental Fate and the Risks Associated with Microcystins in Meiliang Bay, Lake Taihu. Water Res. 2007, 41, 2853-2864. [CrossRef] [PubMed]
35. Chen,W.; Song, L.; Peng, L.;Wan, N.; Zhang, X.; Gan, N. Reduction in microcystin concentrations in large and shallow lakes: Water and Sediment-Interface Contributions. Water Res. 2008, 42, 763-773. [CrossRef] [PubMed]
36. Wang, Q.; Niu, Y.; Xie, P.; Chen, J.; Ma, Z.; Tao, M.; Qi, M.; Wu, L.; Guo, L. Factors affecting temporal and spatial variations of microcystins in Gonghu Bay of Lake Taihu, with potential risk of microcystin contamination to human health. Sci. World J. 2010, 10, 1795-1809. [CrossRef] [PubMed]
37. Otten, T.G.; Paerl, H.W. Phylogenetic inference of colony isolates comprising seasonal Microcystis blooms in Lake Taihu, China. Microb. Ecol. 2011, 62, 907-918. [CrossRef] [PubMed]
38. Wang, X.; Sun, M.; Wang, J.; Yang, L.; Luo, L.; Li, P.; Kong, F. Microcystis genotype succession and related environmental factors in Lake Taihu during cyanobacterial blooms. Microb. Ecol. 2012, 64, 986-999. [CrossRef] [PubMed]
39. Tao, M.; Xie, P.; Chen, J.; Qin, B.; Zhang, D.; Niu, Y.; Zhang, M.; Wang, Q.; Wu, L. Use of a generalized additive model to investigate key abiotic factors affecting microcystin cellular quotas in heavy bloom areas of Lake Taihu. PLoS ONE 2012, 7, e32020. [CrossRef] [PubMed]
40. Liu, Y.; Xie, P.; Zhang, D.; Wen, Z. Seasonal dynamics of microcystins with associated biotic and abiotic parameters in two bays of Lake Taihu, the third largest freshwater lake in China. Bull. Environ. Contam. Toxicol. 2008, 80, 24-29. [CrossRef] [PubMed]
41. Otten, T.G.; Xu, H.; Qin, B.; Zhu, G.; Paerl, H.W. Spatiotemporal patterns and ecophysiology of toxigenic Microcystis blooms in Lake Taihu, China: implications for water quality management. Environ. Sci. Technol. 2012, 46, 3480-3488. [CrossRef] [PubMed]
42. Neilan, B.A.; Jacobs, D.; Blackall, L.L.; Hawkins, P.R.; Cox, P.T.; Goodman, A.E. rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. Int. J. Syst. Bacteriol. 1997, 47, 693-697. [CrossRef] [PubMed]
43. Paerl, H.W.; Xu, H.; McCarthy, M.J.; Zhu, G.; Qin, B.; Li, Y.; Gardner, W. Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): The Need for a Dual Nutrient (N & P) Management Strategy. Water Res. 2011, 45, 1973-1983. [PubMed]
44. Li, D.; Kong, F.; Shi, X.; Ye, L.; Yu, Y.; Yang, Z. Quantification of microcystin-producing and non-microcystin producing Microcystis populations during the 2009 and 2010 blooms in Lake Taihu using quantitative real-time PCR. J. Environ. Sci. 2012, 24, 284-290. [CrossRef]
45. Yu, L.; Kong, F.; Zhang, M.; Yang, Z.; Shi, X.; Du, M. The Dynamics of Microcystis Genotypes and Microcystin Production and Associations with Environmental Factors during Blooms in Lake Chaohu, China. Toxins 2014, 6, 3238-3257. [CrossRef] [PubMed]
46. Zhu, L.; Wu, Y.; Song, L.; Gan, N. Ecological dynamics of toxic Microcystis spp. and microcystin-degrading bacteria in Dianchi Lake, China. Appl. Environ. Microb. 2014, 80, 1874-1881. [CrossRef] [PubMed]
47. Rantala, A.; Rajaniemi-Wacklin, P.; Lyra, C.; Lepisto, L.; Rintala, J.; MankiewiczBoczek, J.; Sivonen, K. Detection of microcystin-producing cyanobacteria in Finnish lakes with genus-specific microcystin synthetase gene E (mcyE) PCR and associations with environmental factors. Appl. Environ. Microb. 2006, 72, 6101-6110. [CrossRef] [PubMed]
48. Rinta-Kanto, J.M.; Konopko, E.A.; DeBruyn, J.M.; Bourbonniere, R.A.; Boyer, G.L.; Wilhelm, S.W. Lake Erie Microcystis: Relationship between Microcystin Production, Dynamics of Genotypes and Environmental Parameters in a Large Lake. Harmful Algae 2009, 8, 665-673. [CrossRef]
49. Zhu, W.; Li, M.; Dai, X.; Xiao, M. Differences in vertical distribution of Microcystis morphospecies composition in a shallow hypertrophic lake (Lake Taihu, China). Environ. Earth Sci. 2015, 73, 5721-5730. [CrossRef]
50. Chan, W.S.; Recknagel, F.; Cao, H.; Park, H.D. Elucidation and short-term forecasting of microcystin concentrations in Lake Suwa (Japan) by means of artificial neural networks and evolutionary algorithms. Water Res. 2007, 41, 2247-2255. [CrossRef] [PubMed]
51. Namikoshi, M.; Rinehart, K.L.; Sakai, R.; Stotts, R.R.; Dahlem, A.M.; Beasley, V.R.; Carmichael, W.W.; Evans, W.R. Identification of 12 hepatotoxins from a Homer Lake bloom of the cyanobacteria Microcystis aeruginosa. Microcystis viridis and Microcystis wesenbergii: Nine New Microcystins. J. Org. Chem. 1992, 57, 866-872. [CrossRef]
52. Otsuka, S.; Suda, S.; Li, R.;Watanabe, M.; Oyaizu, H.;Matsumoto, S.;Watanabe, M. Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence. FEMS Microbiol. Lett. 1999, 172, 15-21. [CrossRef] [PubMed]
53. Ha, J.H.; Hidaka, T.; Tsuno, H. Quantification of toxic Microcystis and evaluation of its dominance ratio in blooms using real-time PCR. Environ. Sci. Technol. 2009, 43, 812-818. [CrossRef] [PubMed]
54. Nusch, E.A. Comparison of different methods for chlorophyll and phaeopigment determination. Archiv. Hydrobiol. Beih. Ergebn. Limnol. 1980, 14, 14-36.
55. Chen, W.; Gan, N.Q.; Song, L.R. Photodegradation dynamics of pure microcystin variants with illumination of fixed wavelength UV-lights. Acta Chim. Sin. 2004, 62, 142-147.