Combined treatment of toxic cyanobacteria Microcystis aeruginosa with hydrogen peroxide and microcystin biodegradation agents results in quick toxins elimination

Dariusz Dziga; Anna Maksylewicz; Magdalena Maroszek; Sylwia Marek

doi:10.18388/abp.2017_2538

Dariusz Dziga Department of Microbiology Faculty of Biochemistry, Biophysics and Biotechnology Jagiellonian University
Anna Maksylewicz Department of Microbiology Faculty of Biochemistry, Biophysics and Biotechnology Jagiellonian University
Magdalena Maroszek Department of Microbiology Faculty of Biochemistry, Biophysics and Biotechnology Jagiellonian University
Sylwia Marek Department of Microbiology Faculty of Biochemistry, Biophysics and Biotechnology Jagiellonian University

DOI: https://doi.org/10.18388/abp.2017_2538

Abstract

In some conditions the growth of toxic cyanobacteria must be controlled by treatment with algicidal compounds. Hydrogen peroxide has been proposed as an efficient and relatively safe chemical which can remove cyanobacteria from the environment selectively, without affecting other microorganisms. However, the uncontrolled release of secondary metabolites, including toxins may occur after such a treatment. Our proposal presented in this paper is fast biodegradation of microcystin released after cell lysis induced by hydrogen peroxide. The effectiveness of both Sphingomonas sp. and heterologously expressed MlrA enzyme in the removal of the toxin from Microcystis aeruginosa culture has been investigated. The results indicate that neither Sphingomonas cells nor MlrA are affected by hydrogen peroxide in the concentrations which stop the growth of cyanobacteria. A several-fold microcystin reduction was documented in the presence of these agents with biodegradation ability. Our results provide evidence that such a combined treatment of water reservoirs dominated by microcystin-producing cyanobacteria may be a promising alternative which allows fast elimination of toxins from the environment.

References

Allahverdiyeva, Y., Isojärvi, J., Zhang, P., Aro, E.-M., (2015). Cyanobacterial Oxygenic Photosynthesis is Protected by Flavodiiron Proteins. Life 5, 716–743. https://doi.org/10.3390/life5010716

Barrington, D.J., Reichwaldt, E.S., Ghadouani, A., (2013). The use of hydrogen peroxide to remove cyanobacteria and microcystins from waste stabilization ponds and hypereutrophic systems. Ecol Eng 50, 86–94. https://doi.org/10.1016/j.ecoleng.2012.04.024

Bourne, D.G., Riddles, P., Jones, G.J., Smith, W., Blakeley, R.L., (2001). Characterisation of a gene cluster involved in bacterial degradation of the cyanobacterial toxin microcystin LR. Environ Toxicol 16, 523–534. https://doi.org/10.1002/tox.10013

Drobac, D., Tokodi, N., Lujić, J., Marinović, Z., Subakov-Simić, G., Dulić, T., Važić, T., Nybom, S., Meriluoto, J., Codd, G.A., Svirčev, Z., (2016). Cyanobacteria and cyanotoxins in fishponds and their effects on fish tissue. Harmful Algae 55, 66–76. https://doi.org/10.1016/j.hal.2016.02.007

Dziga, D., Kokocinski, M., Maksylewicz, A., Czaja-Prokop, U., Barylski, J., (2016a). Cylindrospermopsin biodegradation abilities of Aeromonas sp. isolated from Rusałka Lake. Toxins 8, 1–10. https://doi.org/10.3390/toxins8030055

Dziga, D., Lisznianska, M., Wladyka, B., (2014). Bioreactor study employing bacteria with enhanced activity toward cyanobacterial toxins microcystins. Toxins 6, 2379–2392. https://doi.org/10.3390/toxins6082379

Dziga, D., Wasylewski, M., Szetela, A., Bochenýska, O., Wladyka, B., (2012a). Verification of the role of MlrC in microcystin biodegradation by studies using a heterologously expressed enzyme. Chem Res Toxicol 25, 1192–1194. https://doi.org/10.1021/tx300174e

Dziga, D., Wasylewski, M., Wladyka, B., Nybom, S., Meriluoto, J., (2013). Microbial Degradation of Microcystins. Chem Res Toxicol 26, 841–852.

Dziga, D., Wladyka, B., Zielińska, G., Meriluoto, J., Wasylewski,

M., (2012b). Heterologous expression and characterisation of microcystinase. Toxicon 59, 578–586. https://doi.org/10.1016/j.toxicon.2012.01.001

Dziga, D., Zielinska, G., Wladyka, B., Bochenska, O., Maksylewicz, A., Strzalka, W., Meriluoto, J., (2016b). Characterization of enzymatic activity of MlrB and MlrC proteins involved in bacterial degradation of cyanotoxins microcystins. Toxins 8, 76 https://doi.org/10.3390/toxins8030076

Edwards, C., Graham, D., Fowler, N., Lawton, L.A., (2008). Biodegradation of microcystins and nodularin in freshwaters. Chemosphere 73, 1315–1321. https://doi.org/10.1016/j.chemosphere.2008.07.015

Fan, J., Ho, L., Hobson, P., Brookes, J., (2013). Evaluating the effectiveness of copper sulphate, chlorine, potassium permanganate, hydrogen peroxide and ozone on cyanobacterial cell integrity. Water Res 47, 5153–5164. https://doi.org/10.1016/j.watres.2013.05.057

Fan, J., Hobson, P., Ho, L., Daly, R., Brookes, J., (2014). The effects of various control and water treatment processes on the membrane integrity and toxin fate of cyanobacteria. J Hazard Mater 264, 313–322. https://doi.org/10.1016/j.jhazmat.2013.10.059

Gajdek, P., Lechowski, Z., Bochnia, T., Kepczyński, M., (2001). Decomposition of microcystin-LR by Fenton oxidation. Toxicon 39, 1575–1578. https://doi.org/10.1016/S0041-0101(01)00139-8

Giannuzzi, L., Krock, B., Minaglia, M.C.C., Rosso, L., Houghton, C., Sedan, D., Malanga, G., Espinosa, M., Andrinolo, D., Hernando, M., (2016). Growth, toxin production, active oxygen species and catalase activity of Microcystis aeruginosa (Cyanophyceae) exposed to temperature stress. Comp Biochem Physiol Part - C Toxicol Pharmacol 189, 22–30. https://doi.org/10.1016/j.cbpc.2016.07.001

Huo, X., Chang, D.W., Tseng, J.H., Burch, M.D., Lin, T.F., (2015). Exposure of microcystis aeruginosa to hydrogen peroxide under light: Kinetic modeling of cell rupture and simultaneous microcystin degradation. Environ Sci Technol 49, 5502–5510. https://doi.org/10.1021/acs.est.5b00170

Imanishi, S., Kato, H., Mizuno, M., Tsuji, K., Harada, K.I., (2005). Bacterial degradation of microcystins and nodularin. Chem Res Toxicol 18, 591-598 https://doi.org/10.1021/tx049677g

Iwinski, K.J., Rodgers, J.H., Kinley, C.M., Hendrikse, M.,

Calomeni, A.J., McQueen, A.D., Geer, T.D., Liang, J., Friesen, V., Haakensen, M., (2017). Influence of CuSO4 and chelated copper algaecide exposures on biodegradation of microcystin-LR. Chemosphere 174, 538–544. https://doi.org/10.1016/j.chemosphere.2017.01.079

Kansole, M.M.R., Lin, T.F., (2017). Impacts of hydrogen peroxide and copper sulfate on the control of Microcystis aeruginosa and MC-LR and the inhibition of MC-LR degrading bacterium Bacillus sp. Water 9, 1–18. https://doi.org/10.3390/w9040255

Lawton, L.A., Robertson, P.K.J., Cornish, B.J.P.A., Jaspars, M., (1999). Detoxification of microcystins (cyanobacterial hepatotoxins) using TiO2 photocatalytic oxidation. Environ Sci Technol 33, 771–775. https://doi.org/10.1021/es9806682

Lürling, M., Meng, D., Faassen, E.J., (2014). Effects of hydrogen peroxide and ultrasound on biomass reduction and toxin release in the cyanobacterium, Microcystis aeruginosa. Toxins 6, 3260–3280. https://doi.org/10.3390/toxins6123260

Matthijs, H.C.P., Jančula, D., Visser, P.M., Maršálek, B., (2016). Existing and emerging cyanocidal compounds: new perspectives for cyanobacterial bloom mitigation. Aquat Ecol 50, 443–460. https://doi.org/10.1007/s10452-016-9577-0

Matthijs, H.C.P., Visser, P.M., Reeze, B., Meeuse, J., Slot, P.C., Wijn, G., Talens, R., Huisman, J., (2012). Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide. Water Res 46, 1460–1472. https://doi.org/10.1016/j.watres.2011.11.016

Meriluoto, J., Spoof, L., (2005). Analysis of microcystins by high-performance liquid chromatography with photodiode-array detection, in: Meriluoto, J., Codd, G.A. (Eds.), Toxic Cyanobacterial Monitoring and Cyanotoxin Analysis. Abo Akademi University Press: Turku, Finland, pp. 77–84. https://doi.org/10.1002/9781119068761.ch11

Zhang, M., Pan, G., Yan, H., (2010). Microbial biodegradation of microcystin-RR by bacterium Sphingopyxis sp. USTB-05. J Environ Sci 22, 168–175. https://doi.org/10.1016/S1001-0742(09)60089-9

Zilliges, Y., Kehr, J.C., Meissner, S., Ishida, K., Mikkat, S., Hagemann, M., Kaplan, A., Börner, T., Dittmann, E., (2011). The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of Microcystis under oxidative stress conditions. PLoS One 6, 1–11. https://doi.org/10.1371/journal.pone.0017615