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Journal of Oceanology and Limnology

, Volume 36, Issue 6, pp 2231–2242 | Cite as

The ecological risks of hydrogen peroxide as a cyanocide: its effect on the community structure of bacterioplankton

  • Lizhou Lin (林立洲)
  • Kun Shan (闪锟)
  • Qian Xiong (熊倩)
  • Qichao Zhou (周起超)
  • Lin Li (李林)
  • Nanqin Gan (甘南琴)
  • Lirong Song (宋立荣)
Article
  • 18 Downloads

Abstract

Microcystis blooms are an environmental and ecological concern that has received a serious attention. Hydrogen peroxide (H2O2) is an environment-friendly cyanocide that is commonly used to control Microcystis blooms. While the ecological safety of H2O2 has been previously studied, its influence on bacterioplankton has not been investigated to date. In this study, we used mesocosm experiments to determine the influence of H2O2 on the dynamic changes of the community structure of bacterioplankton. By using deep-sequencing and metagenomics strategy we determined the community structures of phytoplankton and bacterioplankton assemblages that were dominated by Microcystis at a highly eutrophic Dianchi Lake, China. The results showed that Microcystis was more sensitive to H2O2 than other eukaryotic algae. More interestingly, application of H2O2 changed the community structure of bacterioplankton, evidenced by the emergence of Firmicutes as the dominant species in place of Bacteroidetes and Proteobacteria. The H2O2 treatment resulted in the community of bacterioplankton that was primarily dominated by Exiguobacterium and Planomicrobium. Our results show that the abundance changed and the bacterioplankton diversity did not recover even after the concentration of H2O2 reached to the background level. Thus, the response of bacterioplankton must be considered when assessing the ecological risks of using H2O2 to control Microcystis blooms, because bacterioplankton is the key player that forms the basis of food web of aquatic environment.

Keyword

hydrogen peroxide Microcystis bloom ecological risks bacterioplankton 

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Notes

Acknowledgement

We thank Prof. M. Park for his advices and editor’s suggestion of Liwen Bianji, Edanz Group China (www.liwenbianji.ac/ac) for English editing of the revised manuscript.

References

  1. Anbu P, Hur B K, Gyun Lee C. 2013. Isolation and characterization of a novel oxidant–and surfactant–stable extracellular alkaline protease from Exiguobacterium profundum KB–P23. Biotechnology and Applied Biochemistry, 60 (2): 155–161.CrossRefGoogle Scholar
  2. Bagatini I L, Eiler A, Bertilsson S, Klaveness D, Tessarolli L P, Vieira A A H. 2014. Host–specificity and dynamics in bacterial communities associated with bloom–forming freshwater phytoplankton. PLoS One, 9 (1): e85950.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. Barroin G, Feuillade M. 1986. Hydrogen peroxide as a potential algicide for Oscillatoria rubescens D. C. Water Research, 20 (5): 619–623.CrossRefGoogle Scholar
  5. Bishop C T, Anet E F L J, Gorham P R. 1959. Isolation and identification of the fast–death factor in Microcystis aeruginosa NRC–1. Canadian Journal of Biochemistry and Physiology, 37 (3): 453–471.CrossRefGoogle Scholar
  6. Burson A, Matthijs H C P, de Bruijne W, Talens R, Hoogenboom R, Gerssen A, Visser P M, Stomp M, Steur K, van Scheppingen Y, Huisman J. 2014. Termination of a toxic Alexandrium bloom with hydrogen peroxide. Harmful Algae, 31: 125–135.CrossRefGoogle Scholar
  7. Canfield D E, Des Marais D J. 1993. Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochimia et Cosmochimica Acta, 57 (16): 3 971–3 984.CrossRefGoogle Scholar
  8. Casamatta D A, Wickstrom C E. 2000. Sensitivity of two disjunct bacterioplankton communities to exudates from the cyanobacterium Microcystis aeruginosa Kützing. Microbial Ecology, 40 (1): 64–73.CrossRefGoogle Scholar
  9. Cox P A, Sacks O W. 2002. Cycad neurotoxins, consumption of flying foxes, and ALS–PDC disease in Guam. Neurology, 58 (6): 956–959.CrossRefGoogle Scholar
  10. de Kluijver A, Yu J L, Houtekamer M, Middelburg J J, Liu Z W. 2012. Cyanobacteria as a carbon source for zooplankton in eutrophic Lake Taihu, China, measured by 13 C labeling and fatty acid biomarkers. Limnology and Oceanography, 57 (4): 1 245–1 254.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. Gao L, Pan X L, Zhang D Y, Mu S Y, Lee D J, Halik U. 2015. Extracellular polymeric substances buffer against the biocidal effect of H 2 O 2 on the bloom–forming cyanobacterium Microcystis aeruginosa. Water Research, 69: 51–58.CrossRefGoogle Scholar
  13. Glaeser S P, Berghoff B A, Stratmann V, Grossart H P, Glaeser J. 2014. Contrasting effects of singlet oxygen and hydrogen peroxide on bacterial community composition in a humic lake. P L o S One, 9 (3): e92518.CrossRefGoogle Scholar
  14. Häkkinen P J, Anesio A M, Granéli W. 2004. Hydrogen peroxide distribution, production, and decay in boreal lakes. Canadian Journal of Fisheries and Aquatic Sciences, 61 (8): 1 520–1 527.CrossRefGoogle Scholar
  15. Hamilton D P., Salmaso N, Paerl H W. 2016. Mitigating harmful cyanobacterial blooms: strategies for controlof nitrogen and phosphorus loads. Aquatic Ecology, 50 (3): 351–366.CrossRefGoogle Scholar
  16. Harke M J, Steffen M M, Gobler C J, Otten T G, Wilhelm S W, Wood S A, Paerl H W. 2016. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae, 54: 4–20.CrossRefGoogle Scholar
  17. Helman Y, Barkan E, Eisenstadt D, Luz B, Kaplan A. 2005. Fractionation of the three stable oxygen isotopes by oxygen–producing and oxygen–consuming reactions in photosynthetic organisms. Plant Physiology, 138 (4): 2 292–2 298.CrossRefGoogle Scholar
  18. Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T, Schwarz R, Ohad I, Kaplan A. 2003. Genes encoding A–type flavoproteins are essential for photoreduction of O 2 in cyanobacteria. Current Biology, 13 (3): 230–235.CrossRefGoogle Scholar
  19. 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 nextgeneration sequencing–based diversity studies. Nucleic Acids Research, 41 (1): e1.CrossRefGoogle Scholar
  20. Lee D H, Oh K H, Kahng H Y. 2009. Molecular analysis of antioxidant genes in the extremohalophile marine bacterium Exiguobacterium sp. CNU020. Biotechnology Letters, 31 (8): 1 245–1 251.CrossRefGoogle Scholar
  21. Lürling M, Meng D B, Faassen E J. 2014. Effects of hydrogen peroxide and ultrasound on biomass reduction and toxin release in the cyanobacterium, Microcystis aeruginosa. Toxins, 6 (12): 3 260–3 280.CrossRefGoogle Scholar
  22. Magoč T, Salzberg S L. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27 (21): 2 957–2 963.CrossRefGoogle Scholar
  23. Manage P M, Kawabata Z, Nakano S. 2001. Dynamics of cyanophage–like particles and algicidal bacteria causing Microcystis aeruginosa mortality. Limnology, 2 (2): 73–78.CrossRefGoogle Scholar
  24. Matthijs H C P, Jančula D, Visser P M, Maršálek B. 2016. Existing and emerging cyanocidal compounds: new perspectives for cyanobacterial bloom mitigation. Aquat ic Ecology, 50 (3): 443–460.CrossRefGoogle Scholar
  25. 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 R esearch, 46 (5): 1 460–1 472.CrossRefGoogle Scholar
  26. Mehler A H. 1951. Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other hill reagents. Archives of Biochemistry and Biophysics, 33 (1): 65–77.Google Scholar
  27. Paerl H W, Huisman J. 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports, 1 (1): 27–37.CrossRefGoogle Scholar
  28. Porter K G, Feig Y S. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography, 25 (5): 943–948.CrossRefGoogle Scholar
  29. Qin B Q, Xu P Z, Wu Q L, Luo L C, Zhang Y L. 2007. Environmental issues of lake Taihu, China. Hydrobiologia, 581 (1): 3–14.CrossRefGoogle Scholar
  30. Reichwaldt E S, Zheng L, Barrington D J, Ghadouani A. 2012. Acute toxicological response of Daphnia and Moina to hydrogen peroxide. Journal of Environmental Engineering, 138 (5): 607–611.CrossRefGoogle Scholar
  31. Sant’Anna C L, de Carvalho L R, Fiore M F, Silva–Stenico M E, Lorenzi A S, Rios F R, Konno K, Garcia C, Lagos N. 2011. Highly toxic Microcystis aeruginosa strain, isolated from São Paulo–Brazil, produce hepatotoxins and paralytic shellfish poison neurotoxins. Neurotoxicity Research, 19 (3): 389–402.CrossRefGoogle Scholar
  32. Satapathy S, Kumar S, Sukhdane K S, Shukla S P. 2017. Biogenic synthesis and characterization of silver nanoparticles and their effects against bloom–forming algae and synergistic effect with antibiotics against fish pathogenic bacteria. Journal of Applied Phycology, 29 (4): 1 865–1 875.CrossRefGoogle Scholar
  33. Schloss P D, Westcott S L, Ryabin T, Hall J R, Hartmann M, Hollister E B, Lesniewski R A, Oakley B B, Parks D H, Robinson C J, Sahl J W, Stres B, Thallinger G G, van Horn D J, Weber C F. 2009. Introducing mothur: open–source, platform–independent, community–supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75 (23): 7 537–7 541.CrossRefGoogle Scholar
  34. Shan K, Li L, Wang X X, Wu Y L, Hu L L, Yu G L, Song L R. 2014. Modelling ecosystem structure and trophic interactions in a typical cyanobacterial bloom–dominated shallow Lake Dianchi, China. Ecological Modelling, 291: 82–95.CrossRefGoogle Scholar
  35. Shao K Q, Gao G, Chi K X, Qin B Q, Tang X M, Yao X, Dai J Y. 2013. Decomposition of Microcystis blooms: Implications for the structure of the sediment bacterial community, as assessed by a mesocosm experiment in Lake Taihu, China. Journal of Basic Microbiology, 53 (6): 549–554.CrossRefGoogle Scholar
  36. Simon M, Grossart H P, Schweitzer B, Ploug H. 2002. Microbial ecology of organic aggregates in aquatic ecosystems. Aquatic Microbial Ecology, 28: 175–211.CrossRefGoogle Scholar
  37. Stuart T K, Mayali X, Lee J Z, Everroad R C, Hwang M, Bebout B M, Weber P K, Pett–Ridge J, Thelen M P. 2016. Cyanobacterial reuse of extracellular organic carbon in microbial mats. ISME Journal, 10 (5): 1 240–1 251.CrossRefGoogle Scholar
  38. Su J F, Ma M, Wei L, Ma F, Lu J S, Shao S C. 2016. Algicidal and denitrification characterization of Acinetobacter sp. J25 against Microcystis aeruginosa and microbial community in eutrophic landscape water. Marine Pollution Bulletin, 107 (1): 233–239.Google Scholar
  39. Takebe F, Hara I, Matsuyama H, Yumoto I. 2007. Effects of H 2 O 2 under low–and high–aeration level conditions on growth and catalase activity in Exiguobacterium oxidotolerans T–2–2 T. Journal of Bioscience and Bioengineering, 104 (6): 464–469.CrossRefGoogle Scholar
  40. Triest L, Stiers I, van Onsem S. 2016. Biomanipulation as a nature–based solution to reduce cyanobacterial blooms. Aquatic Ecology, 50 (3): 461–483.CrossRefGoogle Scholar
  41. Visser P M, Ibelings B W, Bormans M, Huisman J. 2016. Artificial mixing to controlcyanobacterial blooms: a review. Aquatic Ecology, 50 (3): 423–441.CrossRefGoogle Scholar
  42. Wagner C, Adrian R. 2009. Cyanobacteria dominance: Quantifying the effects of climate change. Limnology and Oceanography, 54 (2): 2 460–2 468.CrossRefGoogle Scholar
  43. Wang B L, Wang X, Hu Y W, Chang M X, Bi Y H, Hu Z Y. 2015a. The combined effects of UV–C radiation and H 2 O 2 on Microcystis aeruginosa, a bloom–forming cyanobacterium. Chemosphere, 141: 34–43.CrossRefGoogle Scholar
  44. Wang S Q, Zhu L, Li Q, Li G B, Li L, Song L R, Gan N Q. 2015b. Distribution and population dynamics of potential anatoxin–a–producing cyanobacteria in Lake Dianchi, China. Harmful Algae, 48: 63–68.CrossRefGoogle Scholar
  45. Wu H M, Wei G J, Tan X, Li L, Li M. 2017. Species–dependent variation in sensitivity of Microcystis species to copper sulfate: implication in algal toxicity of copper and controls of blooms. Scientific Reports, 7: 40 393.CrossRefGoogle Scholar
  46. Wu Y L, Li L, Gan N Q, Zheng L L, Ma H Y, Shan K, Liu J, Xiao B D, Song L R. 2014 Seasonal dynamics of water bloom–forming Microcystis morphospecies and the associated extracellular microcystin concentrations in large, shallow, eutrophic Dianchi Lake. Journal of Environmental Sciences, 26 (9): 1 921–1 929.CrossRefGoogle Scholar
  47. Wu Y L, Li L, Zheng L L, Dai G Y, Ma H Y, Shan K, Wu H D, Zhou Q C, Song L R. 2016. Patterns of succession between bloom–forming cyanobacteria Aphanizomenon flos–aquae and Microcystis and related environmental factors in large, shallow Dianchi Lake, China. Hydrobiologia, 765 (1): 1–13.CrossRefGoogle Scholar
  48. Wu Z X, Gan N Q, Huang Q, Song L R. 2007. Response of Microcystis to copper stress—do phenotypes of Microcystis make a difference in stress tolerance? Environmental Pollution, 147 (2): 324–330.CrossRefGoogle Scholar
  49. Zeng J, Yang L Y, Xiao L, Yin D Q, Qin B Q. 2007. Biogeochemical cycling of nitrogen in lakes and the role of microorganisms in conversion of nitrogen compounds. Journal of Lake Sciences, 19 (4): 382–389. (in Chinese with English abstract)CrossRefGoogle Scholar
  50. Zhang P, Zhai C M, Chen R Q, Liu C H, Xue Y R, Jiang J H. 2012. The dynamics of the water bloom–forming Microcystis aeruginosa and its relationship with biotic and abiotic factors in Lake Taihu, China. Ecological Engineering, 47: 274–277.CrossRefGoogle Scholar
  51. Zhang T, Zheng L L, Li L, Song L R. 2016. 2–Methylisoborneolproduction characteristics of Pseudanabaena sp. FACHB 1277 isolated from Xionghe Reservoir, China. Journal of Applied Phycology, 28 (6): 3 353–3 362.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Lizhou Lin (林立洲)
    • 1
    • 2
  • Kun Shan (闪锟)
    • 1
  • Qian Xiong (熊倩)
    • 1
    • 2
  • Qichao Zhou (周起超)
    • 1
  • Lin Li (李林)
    • 1
  • Nanqin Gan (甘南琴)
    • 1
  • Lirong Song (宋立荣)
    • 1
  1. 1.State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of HydrobiologyChinese Academy of SciencesWuhanChina
  2. 2.University of Chinese Academy of SciencesBeijingChina

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