Environmental Science and Pollution Research

, Volume 26, Issue 31, pp 32255–32265 | Cite as

Control of a toxic cyanobacterial bloom species, Microcystis aeruginosa, using the peptide HPA3NT3-A2

  • Sang-Il Han
  • Sok Kim
  • Ki Young Choi
  • Changsu Lee
  • Yoonkyung ParkEmail author
  • Yoon-E ChoiEmail author
Research Article


Microcystis aeruginosa, a species of freshwater cyanobacteria, is known to be one of the dominant species causing cyanobacterial harmful algal blooms (CyanoHABs). M. aeruginosa blooms have the potential to produce neurotoxins and peptide hepatotoxins, such as microcystins and lipopolysaccharides (LPSs). Currently, technologies for CyanoHAB control do not provide any ultimate solution because of the secondary pollution associated with the control measures. In this study, we attempted to use the peptide HPA3NT3-A2, which has been reported to be nontoxic and has antimicrobial properties, for the development of an eco-friendly control against CyanoHABs. HPA3NT3-A2 displayed significant algicidal effects against M. aeruginosa cells. HPA3NT3-A2 induced cell aggregation and flotation (thereby facilitating harvest), inhibited cell growth through sedimentation, and eventually destroyed the cells. HPA3NT3-A2 had no algicidal effect on other microalgal species such as Haematococcus pluvialis and Chlorella vulgaris. Additionally, HPA3NT3-A2 was not toxic to Daphnia magna. The algicidal mechanism of HPA3NT3-A2 was intracellular penetration. The results of this study suggest the novel possibility of controlling CyanoHABs using HPA3NT3-A2.


Cyanobacterial blooms HABs Microcystis aeruginosa Eco-friendly mitigation Algicide Algicidal peptide HPA3NT3-A2 


Funding information

This work was supported by the Government of South Korea through the National Research Foundation of Korea (NRF-2016R1D1A1B03932773) and Korea Basic Science Institute under the R&D Program (Project No. C38703), supervised by the Ministry of Science, ICT and Future Planning. This research was also supported by the Marine Biotechnology Program of the Korea Institute of Marine Science and Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (MOF) (No. 20170488).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

11356_2019_6306_MOESM1_ESM.docx (108 kb)
ESM 1 (DOCX 108 kb)


  1. Anderson DM (2009) Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast Manag 52(7):342–347Google Scholar
  2. Briand E, Bormans M, Gugger M, Dorrestein PC, Gerwick WH (2016) Changes in secondary metabolic profiles of Microcystis aeruginosa strains in response to intraspecific interactions. Environ Microbiol 18(2):384–400Google Scholar
  3. Chen Y, Li J, Wei J, Kawan A, Wang L, Zhang X (2017) Vitamin C modulates Microcystis aeruginosa death and toxin release by induced Fenton reaction. J Hazard Mater 321:888–895Google Scholar
  4. Cheng L, He Y, Tian Y, Liu B, Zhang Y, Zhou Q, Wu Z (2017) Comparative biotoxicity of N-phenyl-1-naphthylamine and N-phenyl-2-naphthylamine on cyanobacteria Microcystis aeruginosa. Chemosphere 176:183–191Google Scholar
  5. Da Rós PC, Silva CS, Silva-Stenico ME, Fiore MF, de Castro HF (2012) Microcystis aeruginosa lipids as feedstock for biodiesel synthesis by enzymatic route. J Mol Catal B-Enzym 84:177–182Google Scholar
  6. Dolah FMV, Roelke D, Greene RM (2001) Health and ecological impacts of harmful algal blooms: risk assessment needs. Hum Ecol Risk Assess 7(5):1329–1345Google Scholar
  7. Elendt B-P, Bias W-R (1990) Trace nutrient deficiency in Daphnia magna cultured in standard medium for toxicity testing. Effects of the optimization of culture conditions on life history parameters of D. magna. Water Res 24(9):1157–1167Google Scholar
  8. Fábregas J, Domínguez A, Regueiro M, Maseda A, Otero A (2000) Optimization of culture medium for the continuous cultivation of the microalga Haematococcus pluvialis. Appl Microbiol Biotechnol 53(5):530–535Google Scholar
  9. Gorman DS, Levine R (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci U S A 54(6):1665–1669Google Scholar
  10. Gumbo RJ, Ross G, Cloete ET (2008) Biological control of Microcystis dominated harmful algal blooms. Afr J Biotechnol 7(25):4765–4773Google Scholar
  11. Hadjoudja S, Deluchat V, Baudu M (2010) Cell surface characterisation of Microcystis aeruginosa and Chlorella vulgaris. J Colloid Interface Sci 342(2):293–299Google Scholar
  12. Hoiczyk E, Hansel A (2000) Cyanobacterial cell walls: news from an unusual prokaryotic envelope. J Bacteriol 182(5):1191–1199Google Scholar
  13. Hong Y, Hu H-Y, Xie X, Sakoda A, Sagehashi M, Li F-M (2009) Gramine-induced growth inhibition, oxidative damage and antioxidant responses in freshwater cyanobacterium Microcystis aeruginosa. Aquat Toxicol 91(3):262–269Google Scholar
  14. Karlson AM, Mozūraitis R (2011) Deposit-feeders accumulate the cyanobacterial toxin nodularin. Harmful Algae 12:77–81Google Scholar
  15. Kim DG, Lee C, Park S-M, Choi Y-E (2014) Manipulation of light wavelength at appropriate growth stage to enhance biomass productivity and fatty acid methyl ester yield using Chlorella vulgaris. Bioresour Technol 159:240–248Google Scholar
  16. Lee DG, Kim DH, Park Y, Kim HK, Kim HN, Shin YK, Choi CH, Hahm KS (2001a) Fungicidal effect of antimicrobial peptide, PMAP-23, isolated from porcine myeloid against Candida albicans. Biochem Biophys Res Commun 282(2):570–574Google Scholar
  17. Lee T, Nakano K, Matsumara M (2001b) Ultrasonic irradiation for blue-green algae bloom control. Environ Technol 22:383–390Google Scholar
  18. Lee T-H, Hall KN, Swann MJ, Popplewell JF, Unabia S, Park Y, Hahm KS, Aguilar MI (2010) The membrane insertion of helical antimicrobial peptides from the N-terminus of Helicobacter pylori ribosomal protein L1. Biochim Biophys Acta-Biomembr 1798(3):544–557Google Scholar
  19. Lee J-K, Park S-C, Hahm K-S, Park Y (2013) Antimicrobial HPA3NT3 peptide analogs: placement of aromatic rings and positive charges are key determinants for cell selectivity and mechanism of action. Biochim Biophys Acta-Biomembr 1828(2):443–454Google Scholar
  20. Lee J-k, Seo CH, Luchian T, Park Y (2015) The antimicrobial peptide CMA3 derived from the CA-MA hybrid peptide: antibacterial and anti-inflammatory activities with low cytotoxicity and mechanism of action in Escherichia coli. Antimicrob Agents Chemother 60(1):495–506Google Scholar
  21. Lee C, Choi Y-E, Yun Y-S (2016) A strategy for promoting astaxanthin accumulation in Haematococcus pluvialis by 1-aminocyclopropane-1-carboxylic acid application. J Biotechnol 236:120–127Google Scholar
  22. Liu Y, Chen S, Zhang J, Li X, Gao B (2017) Stimulation effects of ciprofloxacin and sulphamethoxazole in Microcystis aeruginosa and isobaric tag for relative and absolute quantitation-based screening of antibiotic targets. Mol Ecol 26(2):689–701Google Scholar
  23. Ma J, Brookes JD, Qin B, Paerl HW, Gao G, Wu P, Zhang W, Deng J, Zhu G, Zhang Y, Xu H, Niu H (2014) Environmental factors controlling colony formation in blooms of the cyanobacteria Microcystis spp. in Lake Taihu, China. Harmful Algae 31:136–142Google Scholar
  24. Manage PM, Zi K, Nakano S-i (2000) Algicidal effect of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat Microb Ecol 22:111–117Google Scholar
  25. Mereuta L, Luchian T, Park Y, Hahm K-S (2008) Single-molecule investigation of the interactions between reconstituted planar lipid membranes and an analogue of the HP (2–20) antimicrobial peptide. Biochem Biophys Res Commun 373(4):467–472Google Scholar
  26. Olli K, Klais R, Tamminen T (2015) Rehabilitating the cyanobacteria–niche partitioning, resource use efficiency and phytoplankton community structure during diazotrophic cyanobacterial blooms. J Ecol 103:1153–1164Google Scholar
  27. Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65(4):995–1010Google Scholar
  28. Paerl HW, Paul VJ (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Res 46(5):1349–1363Google Scholar
  29. Paerl HW, Xu H, McCarthy MJ, Zhu G, Qin B, Li Y, Gardner WS (2011) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Res 45(5):1973–1983Google Scholar
  30. Park S-C, Lee J-K, Kim SW, Park Y (2011) Selective algicidal action of peptides against harmful algal bloom species. PLoS One 6(10):e26733Google Scholar
  31. Qian H, Pan X, Chen J, Zhou D, Chen Z, Zhang L, Fu Z (2012) Analyses of gene expression and physiological changes in Microcystis aeruginosa reveal the phytotoxicities of three environmental pollutants. Ecotoxicology 21(3):847–859Google Scholar
  32. Rao MV, Davis KR (1999) Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J 17(6):603–614Google Scholar
  33. Ren H, Zhang P, Liu C, Xue Y, Lian B (2010) The potential use of bacterium strain R219 for controlling of the bloom-forming cyanobacteria in freshwater lake. World J Microbiol Biotechnol 26(3):465–472Google Scholar
  34. Schopf JW (2000) The fossil record: tracing the roots of the cyanobacterial lineage. In: The ecology of cyanobacteria. Springer, pp 13–35Google Scholar
  35. Stanier R, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35(2):171–205Google Scholar
  36. Sun L-W, Jiang W-J, Sato H, Kawachi M, Lu X-W (2016) Rapid classification and identification of Microcystis aeruginosa strains using MALDI–TOF MS and polygenetic analysis. PLoS One 11:e0156275Google Scholar
  37. Suresh A, Kim YC (2013) Translocation of cell penetrating peptides on Chlamydomonas reinhardtii. Biotechnol Bioeng 110(10):2795–2801Google Scholar
  38. Vives E, Brodin P, Lebleu B (1997) A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 272(25):16010–16017Google Scholar
  39. Wang J, Zhu J, Liu S, Liu B, Gao Y, Wu Z (2011) Generation of reactive oxygen species in cyanobacteria and green algae induced by allelochemicals of submerged macrophytes. Chemosphere 85(6):977–982Google Scholar
  40. Wang G, Deng S, Li C, Liu Y, Chen L, Hu C (2012) Damage to DNA caused by UV-B radiation in the desert cyanobacterium Scytonema javanicum and the effects of exogenous chemicals on the process. Chemosphere 88(4):413–417Google Scholar
  41. Wei Y, Niu J, Huan L, Huang A, He L, Wang G (2015) Cell penetrating peptide can transport dsRNA into microalgae with thin cell walls. Algal Res 8:135–139Google Scholar
  42. Yang C-Y, Liu S-J, Zhou S-W, Wu H-F, Yu J-B, Xia C-H (2011) Allelochemical ethyl 2-methyl acetoacetate (EMA) induces oxidative damage and antioxidant responses in Phaeodactylum tricornutum. Pestic Biochem Physiol 100(1):93–103Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Division of Environmental Science & Ecological EngineeringKorea UniversitySeoulKorea
  2. 2.School of Chemical Engineering, College of EngineeringSungkyunkwan UniversitySuwonKorea
  3. 3.Microbiology and Functionality Research GroupWorld Institute of KimchiGwangjuKorea
  4. 4.Research Center for Proteinaceous Materials (RCPM)Chosun UniversityGwangjuKorea

Personalised recommendations