Abstract
Microcystin, a cyanotoxin produced by Microcystis aeruginosa growing in eutrophic waters, can promote liver tumors in people ingesting contaminated water. To date, water treatment systems have not been effective in removing or degrading these cyanotoxins. In this work, we investigated the inhibitory activity of surfactants on the growth of M. aeruginosa and their application to extract the intracellular produced cyanotoxins. The experiments involving growth inhibition and extraction of cyanotoxins were carried out using the non-biodegradable surfactant cetyl trimethyl ammonium bromide (CTAB) in addition to other biodegradable surfactants. These were Tween 80 and surfactants derived from amino acids and peptides, respectively, from arginine, SDA, and hydrolyzed peptone, SDP. We demonstrated that the tested surfactants could be used to inhibit the growth of M. aeruginosa. At this point, CTAB and SDA proved to be the most competent surfactants in reducing cyanobacterial growth. Moreover, microcystins have been successfully removed from the water employing a cloud point extraction protocol based on the use of these surfactants and ammonium sulfate.




Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Data availability
If requested, we are available to disseminate the data generated in this work.
References
An J, Carmichael WW (1994) Use of a colorimetric protein phosphatase inhibition assay and enzyme linked immunosorbent assay for the study of microcystins and nodularins. Toxicon 32:1495–1507. https://doi.org/10.1016/0041-0101(94)90308-5
Arya SS, Kaimal AM, Chib M, Sonawane SK, Show PL (2019) Novel, energy efficient and green cloud point extraction: technology and applications in food processing. J Food Sci Technol 56:524–534. https://doi.org/10.1007/s13197-018-3546-7
Azevedo SMFO, Carmichael WW, Jochimsen EM, Rinehart KL, Lau S, Shaw GR, Eaglesham GK (2002) Human intoxication by microcystins during renal dialysis treatment in Caruaru – Brazil. Toxicology 181–182:441–446. https://doi.org/10.1016/S0300-483X(02)00491-2
Blanchet-Chouinard G, Larivière D (2018) Determination of Pb in environmental samples after cloud point extraction using crown ether. Talanta 179:300–306. https://doi.org/10.1016/j.talanta.2017.11.015
Bucci AR, Marcelino L, Mendes RK, Etchegaray A (2018) The antimicrobial and antiadhesion activities of micellar solutions of surfactin, CTAB and CPCl with terpinen-4-ol : applications to control oral pathogens. World J Microbiol Biotechnol 34:1–9. https://doi.org/10.1007/s11274-018-2472-1
Carmichael WW (1992) Cyanotoxins secondary metabolites – the cyanotoxins. J Appl Bacteriol 72:445–459
Carmichael WW (1994) The toxins of cyanobacteria. Sci Am 270:78–86. https://doi.org/10.1038/scientificamerican0194-78
Castillo JA, Pinazo A, Carilla J, Infante MR, Alsina MA, Haro I, Clapés P (2004) Interaction of antimicrobial arginine-based cationic surfactants with liposomes and lipid monolayers. Langmuir 20:3379–3387. https://doi.org/10.1021/la036452h
Chandra N, Tyagi VK (2013) Synthesis, properties, and applications of amino acids based surfactants: a review. J Dispers Sci Technol 34:800–808. https://doi.org/10.1080/01932691.2012.695967
Chawla J, Mahajan RK (2011) Cloud point studies of tween and glycol in the presence of salts. J Dispers Sci Technol 32:822–827. https://doi.org/10.1080/01932691.2010.488138
Chen L, Chen J, Zhang X, Xie P (2016) A review of reproductive toxicity of microcystins. J Hazard Mater 301:381–399. https://doi.org/10.1016/j.jhazmat.2015.08.041
Chen H q, Zhao J, Li Y et al (2019) Epigenetic inactivation of LHX6 mediated microcystin-LR induced hepatocarcinogenesis via the Wnt/β-catenin and P53 signaling pathways. Environ Pollut 252:216–226. https://doi.org/10.1016/j.envpol.2019.05.049
Christiansen G, Fastner J, Erhard M et al (2003) Microcystin biosynthesis in planktothrix: genes, evolution, and manipulation. Microbiology 185:564–572. https://doi.org/10.1128/JB.185.2.564
Christophoridis C, Zervou SK, Manolidi K, Katsiapi M, Moustaka-Gouni M, Kaloudis T, Triantis TM, Hiskia A (2018) Occurrence and diversity of cyanotoxins in Greek lakes. Sci Rep 8:1–22. https://doi.org/10.1038/s41598-018-35428-x
Codd GA (2000) Cyanobacterial toxins, the perception of water quality, and the prioritisation of eutrophication control. Ecol Eng 16:51–60. https://doi.org/10.1016/S0925-8574(00)00089-6
Codd G, Bell S, Kaya K, Ward C, Beattie K, Metcalf J (1999) Cyanobacterial toxins, exposure routes and human health. Eur J Phycol 34:405–415. https://doi.org/10.1080/09670269910001736462
Colomer A, Pinazo A, Manresa MA, Vinardell MP, Mitjans M, Infante MR, Pérez L (2011) Cationic surfactants derived from lysine: effects of their structure and charge type on antimicrobial and hemolytic activities. J Med Chem 54:989–1002. https://doi.org/10.1021/jm101315k
Da W, Tao L, Zhu Y (2021) The inhibitory effect of CTAB on human osteosarcoma through the PI3K/AKT signaling pathway. Int J Oncol 59:1–10. https://doi.org/10.3892/ijo.2021.5222
Dai R, Wang P, Jia P et al (2016) A review on factors affecting microcystins production by algae in aquatic environments. World J Microbiol Biotechnol 32:1–7
Dave N, Joshi T (2018) Cloud point analysis: influence of additives on polysorbate. J Dispers Sci Technol 39:548–551. https://doi.org/10.1080/01932691.2017.1334563
Etchegaray A, Rabello E, Dieckmann R, Moon DH, Fiore MF, von Döhren H, Tsai SM, Neilan BA (2004) Algicide production by the filamentous cyanobacterium Fischerella sp. CENA 19. J Appl Phycol 16:237–243. https://doi.org/10.1023/B:JAPH.0000048509.77816.5e
Goldberg J, Kuriyan J, Huang H-B et al (1995) Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1. Nature 376:745–753. https://doi.org/10.1038/376745a0
Gorham PR, McLachlan J, Hammer UT, Kim WK (1964) Isolation and culture of toxic strains of Anabaena flos-aquae (Lyngb.) de Bréb. Int Vereinigung für Theor und Angew Limnol Verhandlungen 15:796–804
Guo N, Jiang YW, Kou P, Liu ZM, Efferth T, Li YY, Fu YJ (2019) Application of integrative cloud point extraction and concentration for the analysis of polyphenols and alkaloids in mulberry leaves. J Pharm Biomed Anal 167:132–139. https://doi.org/10.1016/j.jpba.2019.02.002
Hawkins DR, Rocabayera X, Ruckman S, Segret R, Shaw D (2009) Metabolism and pharmacokinetics of ethyl Nα-lauroyl-L-arginate hydrochloride in human volunteers. Food Chem Toxicol 47:2711–2715. https://doi.org/10.1016/j.fct.2009.07.028
Henriques M, Silva A, Rocha J (2007) Extraction and quantification of pigments from a marine microalga: a simple and reproducible method. In: Méndez-Vilas A (ed) Communicating Current Research and Educational Topics and Trends in Applied Microbiology, Badajoz: FORMATEX, Microbiology series, 1, pp 586–593
Hinojosa MG, Gutiérrez-Praena D, Prieto AI, Guzmán-Guillén R, Jos A, Cameán AM (2019) Neurotoxicity induced by microcystins and cylindrospermopsin: a review. Sci Total Environ 668:547–565. https://doi.org/10.1016/j.scitotenv.2019.02.426
Hinze WL, Pramauro E (1993) A critical review of surfactant-mediated phase separations (cloud-point extractions): theory and applications. Crit Rev Anal Chem 24:133–177. https://doi.org/10.1080/10408349308048821
Hoeger SJ, Dietrich DR, Hitzfeld BC (2002) Effect of ozonation on the removal of cyanobacterial toxins during drinking water treatment. Environ Health Perspect 110:1127–1132. https://doi.org/10.1289/ehp.021101127
Hoeger SJ, Hitzfeld BC, Dietrich DR (2005) Occurrence and elimination of cyanobacterial toxins in drinking water treatment plants. Toxicol Appl Pharmacol 203:231–242. https://doi.org/10.1016/j.taap.2004.04.015
Hudnell HK (2008) Cyanobacterial harmful algal blooms: state of the science and research needs. Springer, New York
Hussain CM, Keçili R (2020) Sampling and sample preparation techniques for environmental analysis. In Hussain CM, Keçili R (ed) Modern environmental analysis techniques for pollutants, Elsevier, pp 75–119
Ito E, Yip KW, Katz D, Fonseca SB, Hedley DW, Chow S, Xu GW, Wood TE, Bastianutto C, Schimmer AD, Kelley SO, Liu FF (2009) Potential use of cetrimonium bromide as an apoptosis-promoting anticancer agent for head and neck cancer. Mol Pharmacol 76:969–983. https://doi.org/10.1124/mol.109.055277
Jia YP, Shi K, Liao JF, Peng JR, Hao Y, Qu Y, Chen LJ, Liu L, Yuan X, Qian ZY, Wei XW (2020) Effects of cetyltrimethylammonium bromide on the toxicity of gold nanorods both in vitro and in vivo: molecular origin of cytotoxicity and inflammation. Small Methods 4:1–11. https://doi.org/10.1002/smtd.201900799
Kachangoon R, Vichapong J, Burakham R, Santaladchaiyakit Y, Srijaranai S (2018) Ultrasonically modified amended-cloud point extraction for simultaneous pre-concentration of neonicotinoid insecticide residues. Molecules 23:(5)1165–1180. https://doi.org/10.3390/molecules23051165
Lai YJS, Zhou Y, Eustance E, Straka L, Wang Z, Rittmann BE (2018) Cell disruption by cationic surfactants affects bioproduct recovery from Synechocystis sp. PCC 6803. Algal Res 34:250–255. https://doi.org/10.1016/j.algal.2018.08.010
Laughinghouse HD, Prá D, Silva-Stenico ME et al (2012) Biomonitoring genotoxicity and cytotoxicity of Microcystis aeruginosa (Chroococcales, cyanobacteria) using the Allium cepa test. Sci Total Environ 432:180–188. https://doi.org/10.1016/j.scitotenv.2012.05.093
Li G, Lan G, Liu Y, Chen C, Lei L, du J, Lu Y, Li Q, du G, Zhang J (2017) Evaluation of biodegradability and biotoxicity of surfactants in soil. 7:31018–31026. https://doi.org/10.1039/c7ra02105d
Liu G, Fan C, Zhong J, Zhang L, Ding S, Yan S, Han S (2010) Using hexadecyl trimethyl ammonium bromide (CTAB) modified clays to clean the Microcystis aeruginosa blooms in Lake Taihu, China. Harmful Algae 9:413–418. https://doi.org/10.1016/j.hal.2010.02.004
Liu JW, Wei KH, Xu SW, Cui J, Ma J, Xiao XL, Xi BD, He XS (2021) Surfactant-enhanced remediation of oil-contaminated soil and groundwater: a review. Sci Total Environ 756:144142. https://doi.org/10.1016/j.scitotenv.2020.144142
Man BKW, Lam MHW, Lam PKS et al (2002) Cloud-point extraction and preconcentration of cyanobacterial toxins (microcystins) from natural waters using a cationic surfactant. Environ Sci Technol 36:3985–3990. https://doi.org/10.1021/es020620v
Masakorala K, Turner A, Brown MT (2011) Toxicity of synthetic surfactants to the marine macroalga, Ulva lactuca. Water Air Soil Pollut 218:283–291. https://doi.org/10.1007/s11270-010-0641-4
Maynes JT, Luu HA, Cherney MM, Andersen RJ, Williams D, Holmes CFB, James MNG (2006) Crystal structures of protein phosphatase-1 bound to motuporin and dihydromicrocystin-LA: elucidation of the mechanism of enzyme inhibition by cyanobacterial toxins. J Mol Biol 356:111–120. https://doi.org/10.1016/j.jmb.2005.11.019
McLellan NL, Manderville RA (2017) Toxic mechanisms of microcystins in mammals. Toxicol Res (Camb) 6:391–405. https://doi.org/10.1039/c7tx00043j
Moldes AB, Rodríguez-López L, Rincón-Fontán M, López-Prieto A, Vecino X, Cruz JM (2021) Synthetic and bio-derived surfactants versus microbial biosurfactants in the cosmetic industry: an overview. Int J Mol Sci 22:1–23. https://doi.org/10.3390/ijms22052371
Morán C, Clapés P, Comelles F, García T, Pérez L, Vinardell P, Mitjans M, Infante MR (2001) Chemical structure/property relationship in single-chain arginine surfactants. Langmuir 17:5071–5075. https://doi.org/10.1021/la010375d
Morán MC, Pinazo A, Pérez L, Clapés P, Angelet M, García MT, Vinardell MP, Infante MR (2004) “Green” amino acid-based surfactants. Green Chem 6:233–240
Nakata K, Tsuchido T, Matsumura Y (2011) Antimicrobial cationic surfactant, cetyltrimethylammonium bromide, induces superoxide stress in Escherichia coli cells. J Appl Microbiol 110:568–579. https://doi.org/10.1111/j.1365-2672.2010.04912.x
Neubauer D, Jaśkiewicz M, Bauer M, Olejniczak-Kęder A, Sikorska E, Sikora K, Kamysz W (2021) Biological and physico-chemical characteristics of arginine-rich peptide gemini surfactants with lysine and cystine spacers. Int J Mol Sci 22:3299. https://doi.org/10.3390/ijms22073299
Nong C, Niu Z, Li P, Wang C, Li W, Wen Y (2017) Dual-cloud point extraction coupled to high performance liquid chromatography for simultaneous determination of trace sulfonamide antimicrobials in urine and water samples. J Chromatogr B Anal Technol Biomed Life Sci 1051:9–16. https://doi.org/10.1016/j.jchromb.2017.02.031
Oberoi J, Dunn DM, Woodford MR, Mariotti L, Schulman J, Bourboulia D, Mollapour M, Vaughan CK (2016) Structural and functional basis of protein phosphatase 5 substrate specificity. Proc Natl Acad Sci 113:9009–9014. https://doi.org/10.1073/pnas.1603059113
Pasupuleti VK, Demain AL (2010) Protein hydrolysates in biotechnology. Springer, Netherlands
Pinazo A, Pons R, Pérez L, Infante MR (2011) Amino acids as raw material for biocompatible surfactants. Ind Eng Chem Res 50:4805–4817. https://doi.org/10.1021/ie1014348
Qazi MJ, Schlegel SJ, Backus EHG, Bonn M, Bonn D, Shahidzadeh N (2020) Dynamic surface tension of surfactants in the presence of high salt concentrations. Langmuir 36(27):7956–7964. https://doi.org/10.1021/acs.langmuir.0c01211
Rai AK, Chaturvedi R, Kumar A (2018) Proteomic evidences for microcystin-RR-induced toxicological alterations in mice liver. Sci Rep 8:1–14. https://doi.org/10.1038/s41598-018-19299-w
Rondel C, Alric I, Mouloungui Z, Blanco JF, Silvestre F (2009) Synthesis and properties of lipoamino acid-fatty acid mixtures: influence of the amphiphilic structure. J Surfactant Deterg 12:269–275. https://doi.org/10.1007/s11743-009-1121-y
Ruckman SA, Rocabayera X, Borzelleca JF, Sandusky CB (2004) Toxicological and metabolic investigations of the safety of N-α-Lauroyl-L-arginine ethyl ester monohydrochloride (LAE). Food Chem Toxicol 42:245–259. https://doi.org/10.1016/j.fct.2003.08.022
Rusinek CA, Bange A, Papautsky I, Heineman WR (2015) Cloud point extraction for electroanalysis: anodic stripping voltammetry of cadmium. Anal Chem 87:6133–6140. https://doi.org/10.1021/acs.analchem.5b00701.
Salton MR (1951) The adsorption of cetyltrimethylammonium bromide by bacteria, its. J Gen Microbiol 5:391–404. https://doi.org/10.1099/00221287-5-2-391
Sant’anna CL, Azevedo MTD (2000) Contribution to the knowledge of potentially toxic cyanobacteria from Brazil. Nova Hedwigia 71:359–385
Schmidt JR, Wilhelm SW, Boyer GL (2014) The fate of microcystins in the environment and challenges for monitoring. Toxins (Basel) 6:3354–3387. https://doi.org/10.3390/toxins6123354
Silva-Stenico ME, Neto RC, Alves IR et al (2009) Hepatotoxin microcystin-LR extraction optimization. J Braz Chem Soc 20:535–542. https://doi.org/10.1590/S0103-50532009000300019
Sivonen K (1996) Cyanobacterial toxins and toxin production. Phycologia 35:12–24. https://doi.org/10.2216/i0031-8884-35-6s-12.1
Strömstedt AAA, Ringstad L, Schmidtchen A, Malmsten M (2010) Interaction between amphiphilic peptides and phospholipid membranes. Curr Opin Colloid Interface Sci 15:467–478. https://doi.org/10.1016/j.cocis.2010.05.006
Tao Y, Brigante M, Zhang H, Mailhot G (2019) Phenanthrene degradation using Fe(III)-EDDS photoactivation under simulated solar light: a model for soil washing effluent treatment. Chemosphere 236:124366. https://doi.org/10.1016/j.chemosphere.2019.124366
Tooming-Klunderud A, Mikalsen B, Kristensen T, Jakobsen KS (2008) The mosaic structure of the mcyABC operon in Microcystis. Microbiology 154:1886–1899. https://doi.org/10.1099/mic.0.2007/015875-0
Tripathy DB, Mishra A, Clark J, Farmer T (2018) Synthesis, chemistry, physicochemical properties and industrial applications of amino acid surfactants: a review. C R Chim 21:112–130. https://doi.org/10.1016/j.crci.2017.11.005
Vaughan M, Van Egmond R (2010) The use of the zebrafish (Danio rerio) embryo for the acute toxicity testing of surfactants, as a possible alternative to the acute fish test. ATLA Altern Lab Anim 38:231–238. https://doi.org/10.1177/026119291003800310
Vences-Guzmán MÁ, Geiger O, Sohlenkamp C (2012) Ornithine lipids and their structural modifications: from A to E and beyond. FEMS Microbiol Lett 335:1–10. https://doi.org/10.1111/j.1574-6968.2012.02623.x
Vieira B, Carmona-ribeiro AM, De Sa U et al (2006) Cationic lipids and surfactants as antifungal agents : mode of action. J Antimicrob Chemother 58:760–767. https://doi.org/10.1093/jac/dkl312
Watanabe H, Tanaka H (1978) A non-ionic surfactant as a new solvent for liquid-liquid extraction of zinc(II) with 1-(2-pyridylazo)-2-naphthol. Talanta 25:585–589. https://doi.org/10.1016/0039-9140(78)80151-9
Welker M, Von Döhren H (2006) Cyanobacterial peptides – nature’s own combinatorial biosynthesis. FEMS Microbiol Rev 30:530–563. https://doi.org/10.1111/j.1574-6976.2006.00022.x
Wu J, Liu H, Huang H, Yuan L, Liu C, Wang Y, Cheng X, Zhuang D, Xu M, Chen X, Losiewicz MD, Zhang H (2019) p53-dependent pathway and the opening of mPTP mediate the apoptosis of co-cultured Sertoli-germ cells induced by microcystin-LR. Environ Toxicol 34:1074–1084. https://doi.org/10.1002/tox.22808
Xing Y, Xu Y, Chen Y, Jeffrey PD, Chao Y, Lin Z, Li Z, Strack S, Stock JB, Shi Y (2006) Structure of protein phosphatase 2A core enzyme bound to tumor-inducing toxins. Cell 127:341–353. https://doi.org/10.1016/j.cell.2006.09.025
Xu Y, Xing Y, Chen Y, Chao Y, Lin Z, Fan E, Yu JW, Strack S, Jeffrey PD, Shi Y (2006) Structure of the protein phosphatase 2A holoenzyme. Cell 127:1239–1251. https://doi.org/10.1016/j.cell.2006.11.033
Yan Y, Li L, Hoffmann H (2006) Clouding: origin of phase separation in oppositely charged polyelectrolyte/surfactant mixed solutions. J Phys Chem B 110:1949–1954. https://doi.org/10.1021/jp056359x
Yu HX, Man BKW, Chan LLN, Lam MHW, Lam PKS, Wang L, Jin H, Wu RSS (2004) Cloud-point extraction of nodularin-R from natural waters. Anal Chim Acta 509:63–70. https://doi.org/10.1016/j.aca.2003.12.019
Yu Q, Zhang B, Ma F, Jia C, Xiao C, Zhang B, Xing L, Li M (2015) Novel mechanisms of surfactants against Candida albicans growth and morphogenesis. Chem Biol Interact 227:1–6. https://doi.org/10.1016/j.cbi.2014.12.014
Zeng G, Fu H, Zhong H, Yuan X, Fu M, Wang W, Huang G (2007) Co-degradation with glucose of four surfactants, CTAB, Triton X-100, SDS and Rhamnolipid, in liquid culture media and compost matrix. Biodegradation 18:303–310. https://doi.org/10.1007/s10532-006-9064-8
Zhao J, Chen H q, Yang H f et al (2019) Epigenetic silencing of ALX4 regulates microcystin-LR induced hepatocellular carcinoma through the P53 pathway. Sci Total Environ 683:317–330. https://doi.org/10.1016/j.scitotenv.2019.05.144
Ziaee F, Ziaee M, Taseidifar M (2021) Synthesis and application of a green surfactant for the treatment of water containing PFAS/hazardous metal ions. J Hazard Mater 407:124800. https://doi.org/10.1016/j.jhazmat.2020.124800
Zingone A, Oksfeldt Enevoldsen H (2000) The diversity of harmful algal blooms: a challenge for science and management. Ocean Coast Manag 43:725–748. https://doi.org/10.1016/S0964-5691(00)00056-9
Funding
This work was supported by the National Council for Scientific and Technological Development (CNPq) [PIBIC/CNPq to T.B.L], Fundo de Apoio à Iniciacao Científica [FAPIC to T.B.L], and PROPESQ (PUC-Campinas).
Author information
Authors and Affiliations
Contributions
Tatiani Brenelli Lima did the experimental work and edited the text. Maria Estela Silva-Stenico ran the mass spectrometry analysis and interpretation. Augusto Etchegaray designed the experiments and edited the manuscript. Marli de Fátima Fiore contributed with her expertise on cyanobacteria and cyanobacterial toxins.
Corresponding author
Ethics declarations
Ethics approval
This article does not include any study with animals or human participants carried out by any of the authors.
Consent to participate
We declare that all authors have consented to participate in this manuscript.
Consent for publication
All authors allow the publication of the paper.
Conflicts of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Vitor Vasconcelos
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Lima, .B., Silva-Stenico, M.E., Fiore, M.F. et al. Microcystins can be extracted from Microcystis aeruginosa using amino acid-derived biosurfactants. Environ Sci Pollut Res 29, 8767–8778 (2022). https://doi.org/10.1007/s11356-021-16257-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16257-4


