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

• Authors: Dariusz Dziga , Anna Maksylewicz , Magdalena Maroszek , Sylwia Marek
• Languages of publication: EN

Abstracts

EN

Under 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 concerns 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 was investigated. The results indicate that neither Sphingomonas cells nor MlrA are affected by hydrogen peroxide at the concentrations which stop the growth of cyanobacteria. A several-fold reduction in microcystin levels 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 both, the bloom forming species and toxins, from the environment.

Keywords

EN

cyanobacteria; microcystins; hydrogen peroxide; microcystinase; Sphingomonas

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2018
• Volume: 65
• Issue: 1
• Pages: 133-140

Dates

published

2018

received

2017-12-01

revised

2018-02-13

accepted

2018-02-13

(unknown)

2018-03-15

Contributors

author

Dariusz Dziga

• Department of Plant Physiology and Development, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland

author

Anna Maksylewicz

• Department of Plant Physiology and Development, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland

author

Magdalena Maroszek

• Department of Plant Physiology and Development, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland

author

Sylwia Marek

• Department of Plant Physiology and Development, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Kraków, Poland

References

• Allahverdiyeva Y, Isojärvi J, Zhang P, Aro EM (2015) Cyanobacterial oxygenic photosynthesis is protected by flavodiiron proteins. Life 5: 716-743. doi: 10.3390/life5010716.
• Barrington DJ, Reichwaldt ES, 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. doi: 10.1016/j.ecoleng.2012.04.024
• Bourne DG, Riddles P, Jones GJ, Smith W, Blakeley RL (2001) Characterisation of a gene cluster involved in bacterial degradation of the cyanobacterial toxin microcystin LR. Environ Toxicol 16: 523-534. doi: 10.1002/tox.10013.
• Drobac D, Tokodi N, Lujić J, Marinović Z, Subakov-Simić G, Dulić T, Vazić T, Nybom S, Meriluoto J, Codd GA, Svirčev Z (2016) Cyanobacteria and cyanotoxins in fishponds and their effects on fish tissue. Harmful Algae 55: 66-76. doi: 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 (Basel) 8: E55. doi: 10.3390/toxins8030055.
• Dziga D, Lisznianska M, Wladyka B (2014) Bioreactor study employing bacteria with enhanced activity toward cyanobacterial toxins microcystins. Toxins (Basel) 6: 2379-2392. doi: 10.3390/toxins6082379.
• Dziga D, Wasylewski M, Szetela A, Bochenska 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. doi: 10.1021/tx300174e.
• Dziga D, Wasylewski M, Wladyka B, Nybom S, Meriluoto J (2013) Microbial degradation of microcystins. Chem Res Toxicol 26: 841-852. doi: 10.1021/tx4000045.
• Dziga D, Wladyka B, Zielińska G, Meriluoto J, Wasylewski M (2012b) Heterologous expression and characterisation of microcystinase. Toxicon 59: 578-586. doi: 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 (Basel) 8: E76. doi: 10.3390/toxins8030076.
• Dziga D, Maksylewicz A, Maroszek M, Budzynska A, Napiorkowska-Krzebietke A, Toporowska M, Grabowska M, Kozak A, Rosińska J, Meriluoto J (2017) The biodegradation of microcystins in temperate freshwater bodies with previous cyanobacterial history. Ecotoxicol Environ Saf 145: 420-430. doi: 10.1016/j.ecoenv.2017.07.046.
• Edwards C, Graham D, Fowler N, Lawton LA (2008) Biodegradation of microcystins and nodularin in freshwaters. Chemosphere 73: 1315-1321. doi: 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. doi: 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. doi: 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. doi: 10.1016/S0041-0101(01)00139-8.
• Giannuzzi L, Krock B, Minaglia MC, 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 C Toxicol Pharmacol 189: 22-30. doi: 10.1016/j.cbpc.2016.07.001.
• Huo X, Chang DW, Tseng JH, Burch MD, Lin TF (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. doi: 10.1021/acs.est.5b00170.
• Imanishi S, Kato H, Mizuno M, Tsuji K, Harada KI (2005) Bacterial degradation of microcystins and nodularin. Chem Res Toxicol 18: 591-598. doi: 10.1021/tx049677g.
• Iwinski KJ, Rodgers JH, Kinley CM, Hendrikse M, Calomeni AJ, McQueen AD, Geer TD, Liang J, Friesen V, Haakensen M (2017) Influence of CuSO4 and chelated copper algaecide exposures on biodegradation of microcystin-LR. Chemosphere 174: 538-544. doi: 10.1016/j.chemosphere.2017.01.079.
• Kansole MMR, Lin TF (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 (Switzerland) 9: 1-18. doi: 10.3390/w9040255
• Lawton LA, Robertson PKJ, Cornish BJPA, Jaspars M (1999) Detoxification of microcystins (cyanobacterial hepatotoxins) using TiO2 photocatalytic oxidation. Environ Sci Technol 33: 771-775. doi: 10.1021/es9806682
• Lürling M, Meng D, Faassen EJ (2014) Effects of hydrogen peroxide and ultrasound on biomass reduction and toxin release in the cyanobacterium, Microcystis aeruginosa. Toxins (Basel) 6: 3260-3280. doi: 10.3390/toxins6123260.
• Matthijs HCP, Jančula D, Visser PM, Maršálek B (2016) Existing and emerging cyanocidal compounds: new perspectives for cyanobacterial bloom mitigation. Aquat Ecol 50: 443-460. doi: 10.1007/s10452-016-9577-0
• Matthijs HC, Visser PM, Reeze B, Meeuse J, Slot PC, Wijn G, Talens R, Huisman J (2012) Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide. Water Res 46: 1460-1472. doi: 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 Toxic Cyanobacterial Monitoring and Cyanotoxin Analysis. Meriluoto J, Codd GA eds, pp 77-84. Abo Akademi University Press. doi: 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 (China) 22: 168-175. doi: 10.1016/S1001-0742(09)60089-9.
• Zilliges Y, Kehr JC, Meissner S, Ishida K, Mikkat S, Hagemann M, Kaplan A, Borner T, Dittmann E (2011) The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of Microcystis under oxidative stress conditions. PLoS ONE 6: e17615. doi: 10.1371/journal.pone.0017615.

Identifiers

DOI

10.18388/abp.2017_2538