Journal of Applied Phycology

, Volume 30, Issue 3, pp 1795–1806 | Cite as

Establishment of a new strategy against Microcystis bloom using newly isolated lytic and toxin-degrading bacteria

  • Changsu Lee
  • Min Seo Jeon
  • Thi-Thao Vo
  • Chulhwan Park
  • Jong-Soon Choi
  • Joseph Kwon
  • Seong Woon Roh
  • Yoon-E Choi


Unwanted, rapid increases in the algal populations of water systems cause harmful algal blooms, which have recently become a major environmental problem. The cyanobacterium Microcystis aeruginosa is the most prevalent bloom species and is responsible for the majority of blooms in freshwater environments. In this study, we attempted to develop an eco-friendly method to suppress M. aeruginosa bloom based on a biological control using bacteria newly isolated from the soil. In a screen for bacteria with strong lethal activity toward Microcystis, we isolated Bacillus sp. T4 and characterised its algicidal activity. Microcystis aeruginosa cells were killed via indirect attack by compound(s) secreted by T4 bacteria. ELISA revealed a dramatic increase in extracellular microcystins in M. aeruginosa cultures upon treatment with T4. Therefore, we screened for bacteria that could degrade these toxins, and three new isolates (R12, S42 and S65) were identified. Simultaneous application of both T4 as a lytic agent and R12 or S42 as toxin-degrading bacteria could eliminate both Microcystis cells and its problematic toxin. Our eco-friendly approach, based on the application of newly isolated bacteria, provides a novel method to control harmful algal blooms.


Algal bloom Cyanobacterium Bacterial isolation Microcystis Biological control Microcystin degradation 



This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) (2016R1D1A1B03932773), the World Institute of Kimchi (KE1802-2), funded by the Ministry of Science and ICT and Korea Basic Science Institute under the R&D program (Project No. C38703) supervised by the Ministry of Science and ICT, Republic of Korea. This work was also supported by the research program of KAERI, Republic of Korea. In addition, this research was supported by Korea University Future Research Grant and Korea University (OJERI) Grant.

Conflict of interest statement

The authors declare no conflict of interest.


  1. Anderson DM (2009) Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast Manag 52:342–347Google Scholar
  2. 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 16:523–534Google Scholar
  3. Chen X, Xiang H, Hu Y, Zhang Y, Ouyang L, Gao M (2013) Fates of Microcystis aeruginosa cells and associated microcystins in sediment and the effect of coagulation process on them. Toxins 6:152–167Google Scholar
  4. Dittmann E, Wiegand C (2006) Cyanobacterial toxins–occurrence, biosynthesis and impact on human affairs. Mol Nutr Food Res 50:7–17Google Scholar
  5. Dziga D, Wasylewski M, Szetela A, Bocheńska O, Wladyka B (2012) Verification of the role of MlrC in microcystin biodegradation by studies using a heterologously expressed enzyme. Chem Res Toxicol 25:1192–1194Google Scholar
  6. Dziga D, Wasylewski M, Wladyka B, Nybom S, Meriluoto J (2013) Microbial degradation of microcystins. Chem Res Toxicol 26:841–852Google Scholar
  7. 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 264:313–322CrossRefPubMedGoogle Scholar
  8. Fontanillo M, Köhn M (2017) Microcystins: synthesis and structure–activity relationship studies toward PP1 and PP2A. Bioorg Med Chem.
  9. Gumbo J, Cloete T, van Zyl G, Sommerville J (2014) The viability assessment of Microcystis aeruginosa cells after co-culturing with Bacillus mycoides B16 using flow cytometry. Phys Chem Earth 72:24–33CrossRefGoogle Scholar
  10. Gumbo RJ, Ross G, Cloete ET (2008) Biological control of Microcystis dominated harmful algal blooms. Afr J Biotechnol 7:4765–4773Google Scholar
  11. Guo X, Liu X, Pan J, Yang H (2015) Synergistic algicidal effect and mechanism of two diketopiperazines produced by Chryseobacterium sp. strain GLY-1106 on the harmful bloom-forming Microcystis aeruginosa. Sci Rep 5:14720CrossRefPubMedPubMedCentralGoogle Scholar
  12. Ho L, Hoefel D, Saint CP, Newcombe G (2007) Isolation and identification of a novel microcystin-degrading bacterium from a biological sand filter. Water Res 41:4685–4695Google Scholar
  13. Jiang Y, Shao J, Wu X, Xu Y, Li R (2011) Active and silent members in the mlr gene cluster of a microcystin-degrading bacterium isolated from Lake Taihu, China. FEMS Microbiol Lett 322 :108–114Google Scholar
  14. Kenefick S, Hrudey S, Peterson H, Prepas E (1993) Toxin release from Microcystis aeruginosa after chemical treatment. Water Sci Technol 27:433–440CrossRefGoogle Scholar
  15. Kim HS, Ahn CY, Joung SH, Ahn JS, Oh HM (2010) Growth inhibition of Microcystis aeruginosa by a glycolipid-type compound from Bacillus subtilis C1. J Microbiol Biotechnol 20:1240–1242Google Scholar
  16. Lee S-O, Kato J, Takiguchi N, Kuroda A, Ikeda T, Mitsutani A, Ohtake H (2000) Involvement of an extracellular protease in algicidal activity of the marine bacterium Pseudoalteromonas sp. strain A28. Appl Environ Microbiol 66:4334–4339Google Scholar
  17. Li H, Ai H, Kang L, Sun X, He Q (2016) Simultaneous Microcystis algicidal and microcystin degrading capability by a single Acinetobacter bacterial strain. Environ Sci Technol 50:11903–11911Google Scholar
  18. Li H, Pan G (2015) Simultaneous removal of harmful algal blooms and microcystins using microorganism-and chitosan-modified local soil. Environ Sci Technol 49:6249–6256Google Scholar
  19. Li Z, Geng M, Yang H (2015) Algicidal activity of Bacillus sp. Lzh-5 and its algicidal compounds against Microcystis aeruginosa. Appl Microbiol Biotechnol 99:981–990Google Scholar
  20. Luo J, Wang Y, Tang S, Liang J, Lin W, Luo L (2013) Isolation and identification of algicidal compound from Streptomyces and algicidal mechanism to Microcystis aeruginosa. PLoS One 8:e76444Google Scholar
  21. Manage PM, Zi K, Nakano S-i (2000) Algicidal effect of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat Microb Ecol 22:111–117CrossRefGoogle Scholar
  22. Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010Google Scholar
  23. Park HD, Sasaki Y, Maruyama T, Yanagisawa E, Hiraishi A, Kato K (2001) Degradation of the cyanobacterial hepatotoxin microcystin by a new bacterium isolated from a hypertrophic lake. Environ Toxicol 16:337–343Google Scholar
  24. Paul C, Pohnert G (2011) Interactions of the algicidal bacterium Kordia algicida with diatoms: regulated protease excretion for specific algal lysis. PLoS One 6:e21032Google Scholar
  25. Saito T, Okano K, Park H-D, Itayama T, Inamori Y, Neilan BA, Burns BP, Sugiura N (2003) Detection and sequencing of the microcystin LR-degrading gene, mlrA, from new bacteria isolated from Japanese lakes. FEMS Microbiol Lett 229:271–276Google Scholar
  26. Shimizu K, Maseda H, Okano K, Kurashima T, Kawauchi Y, Xue Q, Utsumi M, Zhang Z, Sugiura N (2012) Enzymatic pathway for biodegrading microcystin LR in Sphingopyxis sp. C-1. J Biosci Bioeng 114:630–634Google Scholar
  27. Shuang L, Xing L, Yanling Y, Rui W Removal of Microcystis aeruginosa and microcystic toxins by four algaecides. In: 2011th international conference on computer distributed control and intelligent environmental monitoring, 2011. The Institute of Electrical and Electronics Engineers, Changsha, Hunan, China, pp 2189–2192Google Scholar
  28. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729Google Scholar
  29. Wang H, Liu L, Liu ZP, Qin S (2010) Investigations of the characteristics and mode of action of an algalytic bacterium isolated from Tai Lake. J Appl Phycol 22:473–478Google Scholar
  30. World Health Organisation (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. E&FN Spon, London. pp 95–96Google Scholar
  31. World Health Organisation (2004) Guidelines for drinking-water quality. Vol 2. second edn. World Health Organization, Geneva, Switzerland, pp 940–949Google Scholar
  32. Wu L, Wu H, Chen L, Xie S, Zang H, Borriss R, Gao X (2014) Bacilysin from Bacillus amyloliquefaciens FZB42 has specific bactericidal activity against harmful algal bloom species. Appl Environ Microbiol 80:7512–7520Google Scholar
  33. Xuan H, Dai X, Li J, Zhang X, Yang C, Luo F (2017) A Bacillus sp. strain with antagonistic activity against Fusarium graminearum kills Microcystis aeruginosa selectively. Sci Total Environ 583:214–221CrossRefPubMedGoogle Scholar
  34. Yang F, Zhou Y, Sun R, Wei H, Li Y, Yin L, Pu Y (2014) Biodegradation of microcystin-LR and-RR by a novel microcystin-degrading bacterium isolated from Lake Taihu. Biodegradation 25:447–457Google Scholar
  35. Yi Y-L, Yu X-B, Zhang C, Wang G-X (2015) Growth inhibition and microcystin degradation effects of Acinetobacter guillouiae A2 on Microcystis aeruginosa. Res Microbiol 166:93–101Google Scholar
  36. Yu J, Kong Y, Gao S, Miao L, Zou P, Xu B, Zeng C, Zhang X (2015) Bacillus amyloliquefaciens T1 as a potential control agent for cyanobacteria. J Appl Phycol 27:1213–1221Google Scholar
  37. Zhang H, Yu Z, Huang Q, Xiao X, Wang X, Zhang F, Wang X, Liu Y, Hu C (2011) Isolation, identification and characterization of phytoplankton-lytic bacterium CH-22 against Microcystis aeruginosa. Limologica 41:70–77Google Scholar
  38. Zhou S, Shao Y, Gao N, Deng Y, Qiao J, Ou H, Deng J (2013) Effects of different algaecides on the photosynthetic capacity, cell integrity and microcystin-LR release of Microcystis aeruginosa. Sci Total Environ 463:111–119CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Changsu Lee
    • 1
  • Min Seo Jeon
    • 2
  • Thi-Thao Vo
    • 3
  • Chulhwan Park
    • 4
  • Jong-Soon Choi
    • 5
  • Joseph Kwon
    • 5
  • Seong Woon Roh
    • 1
  • Yoon-E Choi
    • 2
  1. 1.Microbiology and Functionality Research Group, World Institute of KimchiGwangjuRepublic of Korea
  2. 2.Division of Environmental Science and Ecological EngineeringCollege of Life Sciences and Biotechnology, Korea UniversitySeoulRepublic of Korea
  3. 3.Department of Bioactive Material SciencesChonbuk National UniversityJeonju-siRepublic of Korea
  4. 4.Department of Chemical EngineeringKwangwoon UniversitySeoulRepublic of Korea
  5. 5.Biological Disaster Analysis Group, Korea Basic Science InstituteDaejeonRepublic of Korea

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