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Simultaneous biodegradation of harmful Cylindrospermopsis raciborskii and cylindrospermopsin toxin in batch culture by single Bacillus strain

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Abstract

This study investigates the capability of a Bacillus flexus strain isolated from decayed cyanobacterial blooms for the bioremediation of Cylindrospermopsis raciborskii and cylindrospermopsin (CYN) toxin. The algicidal activity of this strain was tested by co-cultivation with C. raciborskii cultures. CYN biodegradation was investigated in the presence of living and heat-inactivated bacterial cells or bacterial filtrate. Living bacterial cells inhibited C. raciborskii growth after 2 days of incubation with complete cell death at day 5. Bacterial filtrate caused a rapid reduction in C. raciborskii growth at the first day, with complete cell lysis at day 3. Only living cells of SSZ01 caused reduction in CYN released into the medium during the bacterial decay of C. raciborskii cells. The biodegradation rate of CYN by SSZ01 relied on initial toxin concentrations. The highest rate (42 μg CYN L−1 day−1) was obtained at the higher initial concentration (300 μg L−1), and the lowest (4μg CYN L−1 day−1) was at lower concentration (50 μg L−1). These results suggest that this bacterial strain could be employed to bioremediate cyanobacterial blooms in freshwaters. Also, the application of this bacterium in slow sand filters would give possibilities for degradation and bioremediation of cyanotoxins in drinking water treatment plants.

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References

  • Alamri SA (2012) Biodegradation of microcystin-RR by Bacillus flexus isolated from a Saudi freshwater lake. Saud J Biol Sci 19:435–440

    Article  CAS  Google Scholar 

  • Bazin E, Mourot A, Humpage AR, Fessard V (2010) Genotoxicity of a freshwater cyanotoxin, cylindrospermopsin, in two human cell lines: Caco-2 and HepaRG. Environ Mol Mutagen 51:251–259

    CAS  Google Scholar 

  • Burford MA, Davis TW (2011) Physical and chemical processes promoting dominance of the toxic cyanobacterium Cylindrospermopsis raciborskii. Chin J Oceanol Limnol 29:883–891

    Article  CAS  Google Scholar 

  • Dziga D, Kokocinski M, Maksylewicz A, Czaja-Prokop U, Barylski J (2016) Cylindrospermopsin biodegradation abilities of Aeromonas sp. Isolated from Rusałka Lake. Toxins 8:55

    Article  Google Scholar 

  • Hou X, Huang J, Tang WNA, Zhang LU, Gu L (2019) Allelopathic inhibition of juglone (5-hydroxy-1,4-naphthoquinone) on the growth and physiological performance in Microcystis aeruginosa. J Environ Manag 232:382–386

    Article  CAS  Google Scholar 

  • Hu X, Xu Y, Su HC, Xu WJ, Wang LH, Xu YN, Li ZJ, Yu-Cheng Cao YC, Wen GL (2019) Algicidal bacterium CZBC1 inhibits the growth of Oscillatoria chlorina, Oscillatoria tenuis, and Oscillatoria planctonica. AMB Express 9:144

    Article  Google Scholar 

  • Jebeli MA, Maleki A, Amoozegar MA, Kalantar E, Izanloo H, Gharibi F (2017) Bacillus flexus strain As-12, a new arsenic transformer bacterium isolated from contaminated water resources. Chemosphere 169:636–641

    Article  CAS  Google Scholar 

  • Klitzke S, Apelt S, Weiler C, Fastner J, Chorus I (2010) Retention and degradation of the cyanobacterial toxin cylindrospermopsin in sediments – the role of sediment preconditioning and DOM composition. Toxicon 55:999–1007

    Article  CAS  Google Scholar 

  • Lee C, Jeon MS, Thi-Thao T, Park C, Jong-Soon Choi J, Kwon J, Roh SW, Yoon-E Choi YE (2018) Establishment of a new strategy against Microcystis bloom using newlyisolated lytic and toxin-degrading bacteria. J Appl Phycol 30:1795–1806

    Article  CAS  Google Scholar 

  • Lei L, Dai J, Lin Q, Peng L (2020) Competitive dominance of Microcystis aeruginosa against Raphidiopsis raciborskii is strain- and temperature-dependent. Knowl Manag Aquat Ecosyst 421:36

    Article  Google Scholar 

  • Li N, Zhang L, Li F, Wang Y, Zhu Y, Kang H (2011) Metagenome of microorganisms associated with the toxic cyanobacteria Microcystis aeruginosa analyzed using the 454 sequencing platform. Chin J Oceanol Limnol 29:505–513

    Article  Google Scholar 

  • Luo JF, Wang Y, Tang SS, Liang JW, Lin WT, Luo LX (2013) Isolation and identification of algicidal compound from Streptomyces and algicidal mechanism to Microcystis aeruginosa. PLoS One 8:e76444

    Article  CAS  Google Scholar 

  • Massey IY, Yang F (2020) A mini review on microcystins and bacteria degradation. Toxins 12:268

    Article  CAS  Google Scholar 

  • Mohamed ZA, Alamri SA (2012) Biodegradation of cylindrospermopsin toxin by microcystin- degrading bacteria isolated from cyanobacterial blooms. Toxicon 60:1390–1395

    Article  CAS  Google Scholar 

  • Mohamed ZA, Al-Shehri AM (2007) Cyanobacteria and their toxins in treated-water storage reservoirs in Abha city, Saudi Arabia. Toxicon 50:75–84

    Article  CAS  Google Scholar 

  • Mohamed ZA, Al-Shehri AM (2010) Differential responses of epiphytic and planktonic toxic cyanobacteria to allelopathic substances of the submerged macrophyte stratiotes aloides. Int Rev Hydrobiol 95:224–234

    Article  CAS  Google Scholar 

  • Mohamed ZA, Al-Shehri AM (2013) Assessment of cylindrospermopsin toxin in an arid Saudi lake containing dense cyanobacterial bloom. Environ Monit Assess 185:2157–2166

    Article  CAS  Google Scholar 

  • Mohamed ZA, Deyab MA, Abou-Dobara MI, Kamel A, El-Raghi WM (2015) Occurrence of cyanobacteria and microcystin toxins in raw and treated waters of the Nile River, Egypt: Implication for water treatment and human health. Environ Sci Pollut Res 22:11716–11727

    Article  CAS  Google Scholar 

  • Mohamed ZA, Bakr AA, Ghramh HA (2018) Grazing of the copepod Cyclops vicinus on toxic Microcystis aeruginosa: potential for controlling cyanobacterial blooms and transfer of toxins. Oceanol Hydrobiol Stud 47:296–302

    Article  CAS  Google Scholar 

  • Ndlela LL, Oberholster PJ, Van Wyk JH, Cheng PH (2018) Bacteria as biological control agents of freshwater cyanobacteria: is it feasible beyond the laboratory? Appl Microbiol Biotechnol 102:9911–9923

    Article  CAS  Google Scholar 

  • Nishu SD, Kang Y, Han I, Jung TY, Lee TK (2019) Nutritional status regulates algicidal activity of Aeromonas sp. L23 against cyanobacteria and green algae. PLoS One 14(3):e0213370

    Article  CAS  Google Scholar 

  • Padisak J (1997) Cylindrospermopsisraciborskii (Woloszynska)SeenayaandSubba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of ecology. Arch Hydrobiol 107:563–593

    Google Scholar 

  • Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010

    Article  CAS  Google Scholar 

  • Rücker J, Stüken A, Nixdorf B, Fastner J, Chorus I, Wiedner C (2007) Concentrations of particulate and dissolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes. Toxicon 50:800–809

    Article  Google Scholar 

  • Shao J, Li R, Lepo JE, Gu J-D (2013) Potential for control of harmful cyanobacterial blooms using biologically derived substances: problems and prospects. J Environ Manag 125:149–155

    Article  Google Scholar 

  • Smith MJ, Shaw GR, Eaglesham GK, Ho L, Brookes JD (2008) Elucidating the factors influencing the biodegradation of cylindrospermopsin in drinking water sources. Environ Toxicol 23:413–421

    Article  CAS  Google Scholar 

  • Svircev Z, Obradovic V, Codd GA, Marjanovic P, Spoof L, Drobac D (2016) Massive fish mortality and Cylindrospermopsis raciborskii bloom in Aleksandrovac Lake. Ecotoxicol 25:1353–1363

    Article  CAS  Google Scholar 

  • Tsuji K, Asakawa MY, Anzai T, Sumino T, Harada KI (2006) Degradation of microcystins using immobilized microorganism isolated in an eutrophic lake. Chemosphere 65:117–124

    Article  CAS  Google Scholar 

  • Van Apeldoorn ME, van Egmond HP, Speijers GJA, Bakker GJI (2007) Toxins of cyanobacteria. Mol Nutr Food Res 51:7–60

    Article  Google Scholar 

  • Van Wichelen J, Vanormelingen P, Codd GA, Vyverman W (2016) The common bloom-forming cyanobacterium Microcystis is prone to a wide array of microbial antagonists. Harmful Algae 55:97–111

    Article  Google Scholar 

  • Wang M, Chen S, Zhou W, Yuan W, Wang D (2020) Algal cell lysis by bacteria: a review and comparison to conventional methods. Algal Res 46:101794

    Article  Google Scholar 

  • Weiss G, Kovalerchick D, Lieman-Hurwitz J, Murik O, De Philippis R, Carmeli S, Sukenik A, Kaplan A (2019) Increased algicidal activity of Aeromonas veronii in response to Microcystis aeruginosa: interspecies crosstalk and secondary metabolites synergism. Environ Microbiol 21:1140–1150

    Article  CAS  Google Scholar 

  • Wilkens SL, Maas EW (2012) Development of a novel technique for axenic isolation and culture of Thraustochytrids from New Zealand marine environments. J Appl Microbiol 112:346–352

    Article  CAS  Google Scholar 

  • Wormer L, Cires A, Carrasco D, Quesada A (2008) Cylindrospermopsin is not degraded by co-occurring natural bacterial communities during a 40-day study. Harmful Algae 7:206–213

    Article  Google Scholar 

  • Yang J, Qiao K, Lv J, Liu Q, Nan F, Xie S, Feng J (2020) Isolation and identification of two algae-lysing bacteria against Microcystis aeruginosa. Water 12:2485

    Article  CAS  Google Scholar 

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Acknowledgements

The authors extend their appreciation to the Deanship of Scientific Research, King Khalid University for funding this work through General Research Program under grant number G.R.P.42/42.

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Funding

The authors declare that funding received from Deanship of Scientific Research, King Khalid University for funding this work through General Research Program under grant number G.R.P.42/42, was used in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

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Authors and Affiliations

  1. Faculty of Science, Department of Botany and Microbiology, Sohag University, Sohag, 82524, Egypt

    Zakaria Mohamed

  2. Department of Biology, King Khalid University, College of Science, Abha, 61413, Saudi Arabia

    Saad Alamri & Mohamed Hashem

  3. Faculty of Science, Botany and Microbiology Department, Assiut University, Assiut, 71516, Egypt

    Mohamed Hashem

Authors
  1. Zakaria Mohamed
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  2. Saad Alamri
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  3. Mohamed Hashem
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Contributions

M. H. and S. A. cultured the bacteria strain and followed its growth in biodegradation experiments. Z. M. collected and tabulated data of antialgal and toxin-degrading fungi. Z. M. set up the experiments of algicidal activity of bacteria and biodegradation of toxin in cyanobacterial cultures, and was a major contributor in writing the manuscript. All authors participated in analysis and interpretation of the data, and read and approved the final manuscript.

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Correspondence to Zakaria Mohamed.

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Highlights

• We proved the lytic activity of Bacillus flexus SSZ01against C. raciborskii

• The lytic activity was mediated by bacterial secretion of active metabolites

• Strain SSZ01 can also degrade CYN toxin released from decayed cyanobacterial cells

• This strain could be used as a bioagent to control C. raciborskii bloom in water

• The strain could be applied in slow sand filters to remove CYN from drinking water

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Mohamed, ., Alamri, S. & Hashem, M. Simultaneous biodegradation of harmful Cylindrospermopsis raciborskii and cylindrospermopsin toxin in batch culture by single Bacillus strain. Environ Sci Pollut Res 29, 5153–5161 (2022). https://doi.org/10.1007/s11356-021-16062-z

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  • DOI: https://doi.org/10.1007/s11356-021-16062-z

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