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The effects of electrochemical oxidation on in-vivo fluorescence and toxin content in Microcystis aeruginosa culture

  • ICTC-10 Special Issue: Cyanobacteria and cyanotoxins: responses and detection
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Abstract

The increasing occurrence of cyanobacterial blooms in water bodies is a serious threat to the environment. Efficient in-lake treatment methods for the control of cyanobacteria proliferation are needed, their in-vivo detection to obtain a real-time response to their presence, as well as the information about their physiological state after the applied treatment. In-vivo fluorescence measurements of photosynthetic pigments have proved to be effective for quantitative and qualitative detection of phytoplankton in a water environment. In the experiment, chlorophyll and phycocyanin fluorescence sensors were used concurrently to detect stress caused by electrochemical oxidation applying an electrolytic cell equipped with borondoped diamond electrodes on a laboratory culture of cyanobacteria Microcystis aeruginosa PCC 7806. The inflicted injuries were reflected in a clear transient increase in the phycocyanin fluorescence signal (for 104 %± 43%) 24 h after the treatment, which was not the case for the chlorophyll fluorescence signal. In the next 72 h of observation, the fluorescence signals decreased (on 40% of the starting signal) indicating a reduction of cell number, which was confirmed by cell count (24% reduction of the starting concentration) and analysis of extracted chlorophyll and phycocyanin pigment. These results demonstrate the viability of the combined application of two sensors as a useful tool for in-vivo detection of induced stress, providing real-time information needed for the evaluation of the efficiency of the in-lake treatment and decision upon the necessity of its repetition. The electrochemical treatment also resulted in a lower free microcystins concentration compared to control.

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References

  • Antoniou M G, Shoemaker J A, De La Cruz A A, Dionysiou D D. 2008. Unveiling new degradation intermediates/pathways from the photocatalytic degradation of microcystin-LR. Environmental Science & Technology, 42 (23): 8 877–8 883.

    Article  Google Scholar 

  • Barrington D J, Ghadouani A. 2008. Application of hydrogen peroxide for the removal of toxic cyanobacteria and other phytoplankton from wastewater. Environmental Science & Technology, 42 (23): 8 916–8 921, https://doi.org/10.1021/es801717y.

    Article  Google Scholar 

  • 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. Ecological Engineering, 50: 86–94. https://doi.org/10.1016/j.ecoleng.2012.04.024.

    Article  Google Scholar 

  • Bastien C, Cardin R, Veilleux É, Deblois C, Warren A, Laurion L. 2011. Performance evaluation of phycocyanin probes for the monitoring of cyanobacteria. Journal of Environment Monitoring, 13 (1): 110–118, https://doi.org/10.1039/c0em00366b.

    Article  Google Scholar 

  • Beutler M, Wiltshire K H, Meyer B, Moldaenke C, Lüring C, Meyerhöfer M, Hansen U P, Dau H. 2002. A fluorometric method for the differentiation of algal populations in-vivo and in situ. Photosynthesis Research, 72 (1): 39–53, https://doi.org/10.1023/a:1016026607048.

    Article  Google Scholar 

  • Boopathi T, Ki J S. 2014. Impact of environmental factors on the regulation of cyanotoxin production. Toxins, 6 (7): 1 951–1 978, https://doi.org/10.3390/toxins6071951.

    Article  Google Scholar 

  • Brooks B W, Lazorchak J M, Howard M D A, Johnson M V V, Morton S L, Perkins D A K, Reavie E D, Scott G I, Smith S A, Steevens J A. 2016. Are harmful algal blooms becoming the greatest inland water quality threat to public health and aquatic ecosystems? Environmental Toxicology and Chemistry, 35 (1): 6–13, https://doi.org/10.1002/etc.3220.

    Article  Google Scholar 

  • Bryant D A. 1987. The cyanobacterial photosynthetic apparatus: comparison to those of higher plants and photosynthetic bacteria. Canadian Bulletin of Fisheries and Aquatic Science, 214: 423–500.

    Google Scholar 

  • Cabeza, A, Urtiaga A M, Ortiz I. 2007. Electrochemical treatment of landfill leachates using a boron-doped diamond anode. Industrial & Engineering Chemistry Research, 46 (5): 1 439–1 446, https://doi.org/10.1021/ie061373x.

    Article  Google Scholar 

  • Campbell D, Hurry V, Clarke A K, Gustafsson P, Öquist G. 1998. Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiology and Molecular Biology Reviews, 62 (3): 667–683.

    Google Scholar 

  • Carmichael W W. 1992. Cyanobacteria secondary metabolites-the cyanotoxins. Journal of Applied Bacteriology, 72 (6): 445–459, https://doi.org/10.1111/j.1365-2672.1992.tb01858.x.

    Article  Google Scholar 

  • Chang D W, Hobson P, Burch M, Lin T F. 2012. Measurement of cyanobacteria using in-vivo-fluoroscopy—effect of cyanobacterial species, pigments, and colonies. Water Research, 46 (16): 5 037–5 048, https://doi.org/10.1016/j.watres.2012.06.050.

    Article  Google Scholar 

  • Chen G H. 2004. Electrochemical technologies in wastewater treatment. Separation and Purification Technology, 38 (1): 11–41, https://doi.org/10.1016/j.seppur.2003.10.006.

    Article  Google Scholar 

  • Chorus I, Bartram J. 1999. Toxic Cyanobacteria in water: a guide to their public health consequences, monitoring and management. E&FN Spon, London.

    Google Scholar 

  • Cornish B J P A, Lawton L A, Robertson P K J. 2000. Hydrogen peroxide enhanced photocatalytic oxidation of microcystin-LR using titanium dioxide. Applied Catalysis B: Environmental, 25 (1): 59–67, https://doi.org/10.1016/S0926-3373(99)00121-6.

    Google Scholar 

  • da Silva L M, Santana M H P, Boodts J F C. 2003. Electrochemistry and green chemical processes: electrochemical ozone production. Química Nova, 26 (6): 880–888, https://doi.org/10.1590/S0100-40422003000600017.

    Article  Google Scholar 

  • Daghrir R, Drogui P, Tshibangu J. 2014. Efficient treatment of domestic wastewater by electrochemical oxidation process using bored doped diamond anode. Separation and Purification Technology, 131: 79–83. https://doi.org/10.1016/j.seppur.2014.04.048.

    Article  Google Scholar 

  • Ding Y, Gan N Q, Li J, Sedmak B, Song L R. 2012. Hydrogen peroxide induces apoptotic-like cell death in Microcystis aeruginosa (Chroococcales, Cyanobacteria) in a dosedependent manner. Phycologia, 51: 567–575. https://doi.org/10.2216/11-107.1.

    Article  Google Scholar 

  • Ding Y, Song L R, Sedmak B. 2013. UVB radiation as a potential selective factor favoring microcystin producing bloom forming cyanobacteria. PLoS One, 8 (9): e73919, https://doi.org/10.1371/journal.pone.0073919.

    Article  Google Scholar 

  • Drábková M, Admiraal W, Maršálek B. 2007. Combined exposure to hydrogen peroxide and light-selective effects on cyanobacteria, green algae, and diatoms. Environmental Science & Technology, 41 (1): 309–314, https://doi.org/10.1021/es060746i.

    Article  Google Scholar 

  • Falconer I R. 1989. Effects on human health of some toxic cyanobacteria (blue-green algae) in reservoirs, lakes, and rivers. Toxicity Assessment, 4 (2): 175–184, https://doi.org/10.1002/tox.2540040206.

    Article  Google Scholar 

  • Frontistis Z, Brebou C, Venieri D, Mantzavinos D, Katsaounis A. 2011. BDD anodic oxidation as tertiary wastewater treatment for the removal of emerging micro-pollutants, pathogens and organic matter. Journal of Chemical Technology and Biotechnology, 86 (10): 1 233–1 236, https://doi.org/10.1002/jctb.2669.

    Article  Google Scholar 

  • Fujita Y. 1979. Qualitative and quantitative methods of photosynthetic pigments. In: Nishizawa K, Chihara M eds. Methods in Phycological Studies (Japanese). Kyouritsu Shuppan, Tokyo. p.474–507.

  • Gantt E, Lipschultz CA, Grabowski J, Zimmerman B K. 1979. Phycobilisomes from blue-green and red algae. Plant Physiology, 63 (4): 615–620.

    Article  Google Scholar 

  • García-Montoya M F, Gutiérrez-Granados S, Alatorre-Ordaz A, Galindo R, Ornelas R, Peralta-Hernández J M. 2015. Application of electrochemical/BDD process for the treatment wastewater effluents containing pharmaceutical compounds. Journal of Industrial and Engineering Chemistry, 31: 238–243. https://doi.org/10.1016/j.jiec.2015.06.030.

    Article  Google Scholar 

  • Gregor J, Maršálek B, Šípková H. 2007. Detection and estimation of potentially toxic cyanobacteria in raw water at the drinking water treatment plant by in vivofluorescence method. Water Research, 41 (1): 228–234, https://doi.org/10.1016/j.watres.2006.08.011.

    Article  Google Scholar 

  • Gregor J, Maršálek B. 2004. Freshwater phytoplankton quantification by chlorophyll a: A comparative study of in vitro, in vivo and in situ methods. Water Research, 38 (3): 517–522, https://doi.org/10.1016/j.watres.2003.10.033.

    Article  Google Scholar 

  • Haaken D, Dittmar T, Schmalz V, Worch E. 2012. Influence of operating conditions and wastewater-specific parameters on the electrochemical bulk disinfection of biologically treated sewage at boron-doped diamond (BDD) electrodes. Desalination and Water Treatment, 46 (1–3): 160–167, https://doi.org/10.1080/19443994.2012.677523.

    Article  Google Scholar 

  • Harada K I, Tsuji K. 1998. Persistence and decomposition of hepatotoxic microcystins produced by cyanobacteria in natural environment. Journal of Toxicology-Toxin Reviews, 17 (3): 385–403, https://doi.org/10.3109/15569549809040400.

    Article  Google Scholar 

  • Hilton J, Rigg E, Jaworski G. 1989. Algal identification using in-vivo-fluorescence spectra. Journal of Plankton Research, 11(1): 65–74.

    Article  Google Scholar 

  • ISO. 1992. Water quality-measurement of biochemical parameters-spectrometric determination of the chlorophyll-a concentration: ISO 10260: 1992. Geneva, Switzerland: International Organization for Standardization.

    Google Scholar 

  • Jančula D, Maršálek B. 2011. Critical review of actually available chemical compounds for prevention and management of cyanobacterial blooms. Chemosphere, 85 (9): 1 415–1 422, https://doi.org/10.1016/j.chemosphere.2011.08.036.

    Article  Google Scholar 

  • 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 (4): 871–876, https://doi.org/10.1016/0043-1354(94)90093-0.

    Article  Google Scholar 

  • Lacasa E, Tsolaki E, Sbokou Z, Rodrigo M A, Mantzavinos D, Diamadopoulos E. 2013. Electrochemical disinfection of simulated ballast water on conductive diamond electrodes. Chemical Engineering Journal, 223: 516–523. https://doi.org/10.1016/j.cej.2013.03.003.

    Article  Google Scholar 

  • Lee T, Tsuzuki M, Takeuchi T, Yokoyama K, Karube I. 1994. In-vivo-fluorometric method for early detection of cyanobacterial waterblooms. Journal of Applied Phycology, 6 (5–6): 489–495.

    Article  Google Scholar 

  • Liao W J, Murugananthan M, Zhang Y R. 2014. Electrochemical degradation and mechanistic analysis of microcystin-LR at boron-doped diamond electrode. Chemical Engineering Journal, 243: 117–126. https://doi.org/10.1016/j.cej.2013.12.091.

    Article  Google Scholar 

  • Macário I P E, Castaro B B, Nunes M I S, Antunes S C, Pizarro C, Coelho C, Gonçalves F, de Figueiredo D R. 2015. New insights towards the establishment of phycocyanin concentration thresholds considering species-specific variability of bloom-forming cyanobacteria. Hydrobiologia, 757 (1): 155–165.

    Article  Google Scholar 

  • Martínez-Huitle C A, Brillas E. 2009. Decontamination of wastewaters containing synthetic organic dyes by electrochemical methods: a general review. Applied Catalysis B: Environmental, 87 (3–4): 105–145, https://doi.org/10.1016/j.apcatb.2008.09.017.

    Article  Google Scholar 

  • Martins J, Peixe L, Vasconcelos V M. 2011. Unraveling cyanobacteria ecology in wastewater treatment plants (WWTP). Microbial Ecology, 62 (2): 241–256, https://doi.org/10.1007/s00248-011-9806-y.

    Article  Google Scholar 

  • 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 Research, 46 (5): 1 460–1 472, https://doi.org/10.1016/j.watres.2011.11.016.

    Article  Google Scholar 

  • Meglič A, Pecman A, Rozina T, Leštan D, Sedmak B. 2017. Electrochemical inactivation of cyanobacteria and microcystin degradation using a boron-doped diamond anode-A potential tool for cyanobacterial bloom control. Journal of Environmental Sciences, 53: 248–261. https://doi.org/10.1016/j.jes.2016.02.016.

    Article  Google Scholar 

  • Meriluoto J, Spoof L, Codd G A. 2017. Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis. Wiley, New York. 576p.

    Google Scholar 

  • Oldham P B, Zillioux E J, Warner I M. 1985. Spectral “fingerprinting” of phytoplankton populations by twodimensional fluorescence and Fourier-transform-based pattern recognition. Journal of Marine Research, 43 (4): 893–906.

    Article  Google Scholar 

  • Paerl H W, Hall N S, Calandrino E S. 2011. Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Science of the Total Environment, 409 (10): 1 739–1 745.

    Article  Google Scholar 

  • Paerl H W, Otten T G. 2013. Harmful cyanobacterial blooms: causes, consequences, and controls. Microbial Ecology, 65 (4): 995–1 010, https://doi.org/10.1007/s00248-012-0159-y.

    Article  Google Scholar 

  • Pryor W A. 1986. Oxy-radicals and related species: their formation, lifetimes, and reactions. Annual Review of Physiology, 48: 657–667.

    Google Scholar 

  • Rozina T, Sedmak B, Zupančič Justin M, Meglič A. 2017. Evaluation of cyanobacteria biomass derived from upgrade of phycocyanin fluorescence estimation. Acta Biologica Slovenica, 60(2): 21–28.

    Google Scholar 

  • Samuilov V D, Timofeev K N, Sinitsyn S V, Bezryadnov D V. 2004. H2O2-induced inhibition of photosynthetic O2 evolution by Anabaena variabilis cells. Biochemistry (Moscow), 69 (8): 926–933, https://doi.org/10.1023/B:BIRY.0000040227.66714.19.

    Article  Google Scholar 

  • Schmalz V, Dittmar T, Haaken D, Worch E. 2009. Electrochemical disinfection of biologically treated wastewater from small treatment systems by using borondoped diamond (BDD) electrodes-contribution for direct reuse of domestic wastewater. Water Research, 43 (20): 5 260–5 266, https://doi.org/10.1016/j.watres.2009.08.036.

    Article  Google Scholar 

  • Sedmak B, Carmeli S, Pompe-Novak M, Tušek-Žnidarič M, Grach-Pogrebinsky O, Eleršek T, Žužek M C, Bubik A, Frangež R. 2009. Cyanobacterial cytoskeleton immunostaining: the detection of cyanobacterial cell lysis induced by planktopeptin BL1125. Journal of Plankton Research, 31 (11): 1 321–1 330, https://doi.org/10.1093/plankt/fbp076.

    Article  Google Scholar 

  • Seppälä J, Ylöstalo P, Kaitala S, Hällfors S, Raateoja M, Maunula P. 2007. Ship-of-opportunity based phycocyanin fluorescence monitoring of the filamentous cyanobacteria bloom dynamics in the Baltic Sea. Estuarine, Coastal and Shelf Science, 73 (3–4): 489–500.

    Article  Google Scholar 

  • Sharma V K, Triantis T M, Antoniou M G, He X X, Pelaez M, Han C, Song W H, O’Shea K E, de la Cruz A A, Kaloudis T, Hiskia A, Dionysiou D D. 2012. Destruction of microcystins by conventional and advanced oxidation processes: a review. Separation and Purification Technology, 91: 3–17. https://doi.org/10.1016/j.seppur.2012.02.018.

    Article  Google Scholar 

  • Svirčev Z, Drobac D, Tokodi N, Mijović B, Codd G A, Meriluoto J. 2017. Toxicology of microcystins with reference to cases of human intoxications and epidemiological investigations of exposures to cyanobacteria and cyanotoxins. Archives of Toxicology, 91 (2): 621–650, https://doi.org/10.1007/s00204-016-1921-6.

    Article  Google Scholar 

  • Tsuji K, Watanuki T, Kondo F, Watanabe M F, Nakazawa H, Suzuki M, Uchida H, Harada K I. 1997. Stability of microcystins from cyanobacteria-iv. effect of chlorination on decomposition. Toxicon, 35 (7): 1 033–1 041.

    Article  Google Scholar 

  • van Hullebusch E D, Zandvoort M H, Lens P N L. 2003. Metal immobilisation by biofilms: mechanisms and analytical tools. Reviews in Environmental Science and Biotechnology, 2 (1): 9–33.

    Article  Google Scholar 

  • Wlodarczyk L M, Moldaenke C, Fiedor L. 2012. Fluorescence as a probe for physiological integrity of freshwater cyanobacteria. Hydrobiologia, 695 (1): 73–81, https://doi.org/10.1007/s10750-012-1122-0.

    Article  Google Scholar 

  • Yamamoto Y, Nakahara H. 2009. Seasonal variations in the morphology of bloom-forming cyanobacteria in a eutrophic pond. Limnology, 10 (3): 185–193, https://doi.org/10.1007/s10201-009-0270-z.

    Article  Google Scholar 

  • Yang Z, Kong F X, Shi X L, Yu Y, Zhang M. 2015. Effects of UV-B radiation on microcystin production of a toxic strain of Microcystis aeruginosa and its competitiveness against a non-toxic strain. Journal of Hazardous Materials, 283: 447–453.

    Article  Google Scholar 

  • Yentsch C S, Yentsch C M. 1979. Fluorescence spectral signatures: the characterization of phytoplankton population by the use of excitation and emission spectra. Journal of Marine Research, 37 (3): 471–483.

    Google Scholar 

  • Zhang C Y, Fu D G, Gu Z Z. 2009. Degradation of microcystin-RR using boron-doped diamond electrode. Journal of Hazardous Materials, 172 (2–3): 847–853, https://doi.org/10.1016/j.jhazmat.2009.07.071.

    Article  Google Scholar 

  • Zilinskas B A, Glick R E. 1981. Noncovalent intermolecular forces in phycobilisomes of Porphyridium cruentum. Plant Physiology, 68 (2): 447–452.

    Article  Google Scholar 

  • Zupančič Justin M, Gerl M, Lakovič G, Sedmak B, Rozina T, Finžgar N, Čič M, Marinović M, Teslić L, Grum J, Čater M, Eleršek T, Meglič A, Yakuntsov A, Pokorn L, Kralj T, Berčon M, Hamiti B. 2017. LIFE stop cyanoBloom: innovative technology for cyanobacterial bloom control: LIFE12 ENV/SI/000783. Arhel d.o.o., National Institute of Biology and Municipality Bled, Slovenia, https://doi.org/lifestopcyanobloom.arhel.si/wp-content/uploads/LIFE-12ENVSI783-Stop-CyanoBloom-Technical-Report-forpublication.pdf.

    Google Scholar 

  • Zurawell R W, Chen H R, Burke J M, Prepas E E. 2005. Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. Journal of Toxicology and Environmental Health, Part B, 8 (1): 1–37, https://doi.org/10.1080/10937400590889412.

    Article  Google Scholar 

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Acknowledgement

The authors are grateful to the Engineering team of Arhel d.o.o., Gorazd Lakovič and Marko Gerl, for the development and assistance in the use of sensor equipment and an electrolytic cell.

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Correspondence to Maja Zupančič Justin.

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Supported by the ARRS Project L1-5456 (Control of Harmful Cyanobacteria Bloom in Fresh-Water Bodies) and LIFE + Project: LIFE12 ENV/SI/00083 LIFE Stop CyanoBloom

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Rozina, T., Eleršek, T., Zupančič Justin, M. et al. The effects of electrochemical oxidation on in-vivo fluorescence and toxin content in Microcystis aeruginosa culture. J. Ocean. Limnol. 36, 1091–1102 (2018). https://doi.org/10.1007/s00343-019-7180-7

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