Microcystin-LR Degradation Following Copper-Based Algaecide Exposures

  • Ciera M. Kinley
  • Kyla J. Iwinski-Wood
  • Tyler D. Geer
  • Maas Hendrikse
  • Andrew D. McQueen
  • Alyssa J. Calomeni
  • Jenny Liang
  • Vanessa Friesen
  • Monique C. Simair
  • John H. RodgersJr
Article
  • 66 Downloads

Abstract

When copper-based algaecides are used in aquatic systems to decrease cyanobacteria densities, endotoxin fate is a concern, due to the potential for human health and ecological risks. Pulse exposures of algaecides can result in episodic low dissolved oxygen (DO) concentrations (< 2 mg L−1), due to oxygen consumed via microbial oxidation of algal detritus. Research objectives of this study were to determine the influence of declining DO levels on microcystin-LR (MC-LR) degradation and changes in resident bacterial assemblages. It was hypothesized that cyanobacteria cell densities would be positively correlated with rates and extents of DO decline based on the oxygen required for bacteria to degrade cyanobacteria detritus following exposure to copper-based algaecides. In addition, it was hypothesized that total MC-LR concentrations would increase proportionally with increasing cyanobacteria cell densities. Mesocosm experiments were conducted in a pond in Anderson, SC, that frequently experiences cyanobacteria blooms. Three densities of a cyanobacteria assemblage were exposed to a copper ethanolamine algaecide. DO and total MC-LR concentrations were measured with time following algaecide exposures to determine rates and extents of declines. As anticipated, DO concentrations had the highest rate of decline in the highest cell density treatment, followed by medium and low cell densities. MC-LR degradation occurred at similar rates (half-lives 1 to 1.9 days) among cell densities. Acinetobacter and Aeromonas were dominant in treatments following copper exposures. The relationship between cyanobacteria densities and MC-LR half-lives demonstrates the benefits of managing cyanobacteria in early growth stages to minimize MC concentrations.

Keywords

Microcystin-LR Biodegradation Copper-algaecide Oxygen demand Cyanobacteria 

Notes

Acknowledgments

The authors thank Lonza for financial support for this research. Thank you to Dr. Wayne Chao of Clemson University for analytical assistance. The authors also thank Bill Ratajczyk and Dr. Ryan Wersal for review of this manuscript.

Supplementary material

11270_2018_3729_MOESM1_ESM.docx (12 kb)
ESM 1 (DOCX 12 kb)
11270_2018_3729_MOESM2_ESM.docx (114 kb)
ESM 2 (DOCX 113 kb)

References

  1. American Public Health Association (APHA). (2012). Standard methods for the examination of water and wastewater (21th ed.). Washington, DC: American Public Health Association.Google Scholar
  2. Azevedo, S. M., Carmichael, W. W., Jochimsen, E. M., Rinehart, K. L., Lau, S., Shaw, G. R., & Eaglesham, G. K. (2002). Human intoxication by microcystins during renal dialysis treatment in Caruaru—Brazil. Toxicology, 181, 441–446.CrossRefGoogle Scholar
  3. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335–336.CrossRefGoogle Scholar
  4. Carpenter, S. R., Caraco, N. F., Correll, D. L., Howarth, R. W., Sharpley, A. N., & Smith, V. H. (1998). Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecological Applications, 8, 559–568.CrossRefGoogle Scholar
  5. Chen, W., Song, L., Peng, L., Wan, N., Zhang, X., & Gan, N. (2008). Reduction in microcystin concentrations in large and shallow lakes: water and sediment-interface contributions. Water Research, 42, 763–773.CrossRefGoogle Scholar
  6. Chen, X., Yang, X., Yang, L., Xiao, B., Wu, X., Wang, J., & Wan, H. (2010). An effective pathway for the removal of microcystin LR via anoxic biodegradation in lake sediments. Water Research, 44, 1884–1892.CrossRefGoogle Scholar
  7. Chen, J., Han, F. X., Wang, F., Zhang, H., & Shi, Z. (2012). Accumulation and phytotoxicity of microcystin-LR in rice (Oryza sativa). Ecotoxicology and Environmental Safety, 76, 193–199.CrossRefGoogle Scholar
  8. Chorus, I., & Bartram, J. (1999). Toxic cyanobacteria in water: a guide to public health significance. London: World Health Organization, E&FN Spon.CrossRefGoogle Scholar
  9. Corbel, S., Mougin, C., & Bouaïcha, N. (2014). Cyanobacterial toxins: modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere, 96, 1–15.CrossRefGoogle Scholar
  10. Cousins, I. T., Bealing, D. J., James, H. A., & Sutton, A. (1996). Biodegradation of microcystin-LR by indigenous mixed bacterial populations. Water Research, 30, 481–485.CrossRefGoogle Scholar
  11. DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology, 72, 5069–5072.CrossRefGoogle Scholar
  12. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460–2461.CrossRefGoogle Scholar
  13. Edwards, C., Graham, D., Fowler, N., & Lawton, L. A. (2008). Biodegradation of microcystins and nodularin in freshwaters. Chemosphere, 73(8), 1315–1321.CrossRefGoogle Scholar
  14. Fawell, J. K., Mitchell, R. E., Everett, D. J., & Hill, R. E. (1999). The toxicity of cyanobacterial toxins in the mouse: I microcystin-LR. Human & Experimental Toxicology, 18, 162–167.CrossRefGoogle Scholar
  15. Graney, R. L., J. P. Giesy, & Clark, J. R.. (1995). Field studies. In: Fundamental of aquatic toxicology: Effects, environmental fate and risk assessment (pp. 257–304).Google Scholar
  16. Grenz, C., Cloern, J. E., Hager, S. W., & Cole, B. E. (2000). Dynamics of nutrient cycling and related benthic nutrient and oxygen fluxes during a spring phytoplankton bloom in South San Francisco Bay (USA). Marine Ecology Progress Series, 67–80.Google Scholar
  17. Henriksen, S. D. (1976). Moraxella, Neisseria, Branhamella, and Acinetobacter. Annual Reviews in Microbiology, 30, 63–83.CrossRefGoogle Scholar
  18. Himedia Labs (2011). R2-A Broth M1687. Retrieved from: http://himedialabs.com/TD/M1687.pdf
  19. Holst, T., Jørgensen, N. O., Jørgensen, C., & Johansen, A. (2003). Degradation of microcystin in sediments at oxic and anoxic, denitrifying conditions. Water Research, 37, 4748–4760.CrossRefGoogle Scholar
  20. Iwinski, K. J. (2016). Release and degradation of Microcystin-LR following exposures of Microcystis to copper-based algaecides (Doctoral dissertation, Clemson University).Google Scholar
  21. Iwinski, K. J., Calomeni, A. J., Geer, T. D., & Rodgers, J. H. (2016). Cellular and aqueous microcystin-LR following laboratory exposures of Microcystis aeruginosa to copper algaecides. Chemosphere, 147, 74–81.CrossRefGoogle Scholar
  22. Iwinski, K. J., Rodgers, J. H., Kinley, C. M., Hendrikse, M., Calomeni, A. J., McQueen, A. D., et al. (2017). Influence of CuSO4 and chelated copper algaecide exposures on biodegradation of microcystin-LR. Chemosphere, 174, 538–544.CrossRefGoogle Scholar
  23. Jones, G. J., & Orr, P. T. (1994). Release and degradation of microcystin following algicide treatment of a Microcystis aeruginosa bloom in a recreational lake, as determined by HPLC and protein phosphatase inhibition assay. Water Research, 28, 871–876.CrossRefGoogle Scholar
  24. Juni, E. (1978). Genetics and physiology of Acinetobacter. Annual Reviews in Microbiology, 32, 349–371.CrossRefGoogle Scholar
  25. Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., & Glöckner, F. O. (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research, 41(1), e1–e1.CrossRefGoogle Scholar
  26. Lam, A. K. Y., Fedorak, P. M., & Prepas, E. E. (1995). Biotransformation of the cyanobacterial hepatotoxin microcystin-LR, as determined by HPLC and protein phosphatase bioassay. Environmental Science & Technology, 29(1), 242–246.Google Scholar
  27. Lee, Y. J., Jung, J. M., Jang, M. H., Ha, K., & Joo, G. J. (2006). Degradation of microcystins by adsorbed bacteria on a granular active carbon(GAC) filter during the water treatment process. Journal of Environmental Biology, 37(2), 317–322.Google Scholar
  28. Li, H., Ai, H., Kang, L., Sun, X., & He, Q. (2016). Simultaneous Microcystis Algicidal and microcystin degrading capability by a single Acinetobacter bacterial strain. Environmental Science & Technology, 50, 11903–11911.CrossRefGoogle Scholar
  29. Lötter, L. H. (1985). The role of bacterial phosphate metabolism in enhanced phosphorus removal from the activated sludge process. Water Science and Technology, 17(11–12), 127–138.Google Scholar
  30. Lötter, L. H., & Murphy, M. (1985). The identification of heterotrophic bacteria in an activated sludge plant with particular reference to polyphosphate accumulation. Water SA, 11(4), 179–184.Google Scholar
  31. Lötter, L. H., Wentzel, M. C., Loewenthal, R. E., Ekama, G. A., & Marais, G. (1986). A study of selected characteristics of Acinetobacter spp. isolated from activated sludge in anaerobic/anoxic/aerobic and aerobic systems. Water SA, 12(4), 203–208.Google Scholar
  32. Masella, A. P., Bartram, A. K., Truszkowski, J. M., Brown, D. G., & Neufeld, J. D. (2012). PANDAseq: PAired-eND assembler for Illumina sequences. BMC Bioinformatics, 13, 31.CrossRefGoogle Scholar
  33. McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., et al. (2012). An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. The ISME Journal, 6, 610–618.CrossRefGoogle Scholar
  34. Sawyer, C. N., & McCarty, P. L. (1967). Chemistry for sanitary engineers. In Chemistry for sanitary engineers. McGraw-Hill.Google Scholar
  35. Stewart, I., Seawright, A. A., & Shaw, G. R. (2008). Cyanobacterial poisoning in livestock, wild mammals and birds—an overview. In Cyanobacterial harmful algal blooms: state of the science and research needs (pp. 613–637). New York: Springer.Google Scholar
  36. Tsao, S., Wei, D. J., Chang, Y. T., & Lee, J. F. (2017). Aerobic biodegradation of microcystin-LR by an indigenous bacterial mixed culture isolated in Taiwan. International Biodeterioration & Biodegradation, 124, 101–108.CrossRefGoogle Scholar
  37. United States Environmental Protection Agency (USEPA). (2015). Drinking water health advisory for the cyanobacterial microcystin toxins. Office of Water 4304T. EPA-820R15100.Google Scholar
  38. Varma, M. M., & DiGiano, F. (1968). Kinetics of oxygen uptake by dead algae. Journal of the Water Pollution Control Federation, 613–626.Google Scholar
  39. Watanabe, M. F., Tsuji, K., Watanabe, Y., Harada, K. I., & Suzuki, M. (1992). Release of heptapeptide toxin (microcystin) during the decomposition process of Microcystis aeruginosa. Natural Toxins, 1, 48–53.CrossRefGoogle Scholar
  40. Wetzel, R. G. (2001). Limnology: lakes and river ecosystems. Boca Raton, FL: Gulf Professional Publishing.Google Scholar
  41. World Health Organization (WHO). (2011). Guidelines for drinking water quality (4th ed.). Geneva: World Health Organization (http://www.who.int/water_sanitation_health/publications/2011/dwq_chapters/en).Google Scholar
  42. Zimba, P. V., Khoo, L., Gaunt, P. S., Brittain, S., & Carmichael, W. W. (2001). Confirmation of catfish, Ictalurus punctatus (Rafinesque), mortality from Microcystis toxins. Journal of Fish Diseases, 24, 41–47.CrossRefGoogle Scholar
  43. Zohary, T., & Madeira, A. M. (1990). Structural, physical and chemical characteristics of Microcystis aeruginosa hyperscums from a hypertrophic lake. Freshwater Biology, 23, 339–352.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Ciera M. Kinley
    • 1
  • Kyla J. Iwinski-Wood
    • 2
  • Tyler D. Geer
    • 1
  • Maas Hendrikse
    • 1
  • Andrew D. McQueen
    • 3
  • Alyssa J. Calomeni
    • 1
  • Jenny Liang
    • 4
  • Vanessa Friesen
    • 4
  • Monique C. Simair
    • 4
  • John H. RodgersJr
    • 1
  1. 1.Department of Forestry and Environmental ConservationClemson UniversityClemsonUSA
  2. 2.Applied Polymer SystemsWoodstockUSA
  3. 3.Engineer Research and Development CenterUS Army Corps of EngineersVicksburgUSA
  4. 4.Contango Strategies Ltd.SaskatoonCanada

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