Advertisement

Environmental Science and Pollution Research

, Volume 26, Issue 5, pp 4878–4889 | Cite as

Reduced ecotoxicity and improved biodegradability of cationic biocides based on ester-functionalized pyridinium ionic liquids

  • Maria Trush
  • Larysa Metelytsia
  • Ivan Semenyuta
  • Larysa Kalashnikova
  • Oleksiy Papeykin
  • Irina Venger
  • Oksana Tarasyuk
  • Larysa Bodachivska
  • Volodymyr Blagodatnyi
  • Sergiy RogalskyEmail author
Research Article
First Online:
  • 95 Downloads

Abstract

Ester-functionalized pyridinium ionic liquids (ILs), 1-decyloxycarbonylmethylpyridinium chloride (PyrСOOC10-Cl), and 1-dodecyloxycarbonylmethylpyridinium chloride (PyrСOOC12-Cl) have been synthesized and studied for their environmental toxicity. Simple long-chain pyridinium ILs, 1-dodecylpyridinium chloride (PyrC12-Cl), and commercial disinfectant cetylpyridinium chloride (CPC) were used as reference compounds. Both ester-functionalized ILs and CPC showed significantly reduced antibacterial activity compared to PyrC12-Cl. However, ester-functionalized ILs were found to have excellent antifungal activity towards Candida albicans fungus strains, similar to PyrC12-Cl and much higher than for CPC. The molecular docking of ILs in the active site of the known antifungal target N-myristoyltransferase (Nmt) C. albicans has been conducted. The obtained results indicate the possibility of ILs binding into the Nmt pocket. The high stability of the complexes, especially for PyrCOOC10-Cl, is ensured by hydrogen bonding, electrostatic anion-pi interactions, as well as hydrophobic pi-alkyl and alkyl interactions that was confirmed by calculated binding energy values. The acute toxicity studies of ester-functionalized ILs on D. rerio (zebrafish) hydrobiont have shown their dramatically reduced ecotoxicity compared to PyrC12-Cl and CPC. Thus, LD50 values of 15.2 mg/L and 16.8 mg/L were obtained for PyrCOOC10-Cl and PyrCOOC12-Cl, respectively, whereas CPC had LD50 value of 0.018 mg/L. The primary biodegradation test CEC L-33-A93 of ILs indicated an improved biodegradability of ester-functionalized compounds compared to simple long-chain ILs. Based on the obtained results, PyrCOOC10-Cl may be considered as very promising cationic biocide due to the combination of soft antimicrobial activity and reduced ecotoxicity, as well as improved biodegradability.

Keywords

Pyridinium ionic liquids Ester-functionalized Antimicrobial activity Molecular docking, N-myristoyltranferase, ecotoxicity, biodegradability 
This is a preview of subscription content, log in to check access.

References

  1. Al-Rawashded NAF, Maayta AK (2005) Cationic surfactant as corrosion inhibitor for aluminum in acidic and basic solutions. Anti-Corrosion Methods and Materials 52(3):160–166.  https://doi.org/10.1108/00035590510595157 CrossRefGoogle Scholar
  2. Arning J, Stolte S, Böschen A, Stock F, Pitner W-R, Welz-Biermann U, Jastorff B, Ranke J (2008) Qualitative and quantitative structure activity relationships for the inhibitory effects of cationic head groups, functionalised side chains and anions of ionic liquids on acetylcholinesterase. Green Chem 10:47–58.  https://doi.org/10.1039/B712109A CrossRefGoogle Scholar
  3. Battersby NS, Morgan P (1997) A note on the use of the CEC L-33-A-93 test to predict the potential biodegradation of mineral oil based lubricants in soil. Chemosphere 35:1773–1779.  https://doi.org/10.1016/S0045-6535(97)00240-3 CrossRefGoogle Scholar
  4. Bauer A, Kirby W, Sherris J, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496 PMID: 5325707CrossRefGoogle Scholar
  5. Bergamo VZ, Donato RK, Dalla Lana DF, Donato KJZ, Ortega GG, Schrekker HS, Fuentefria AM (2014) Imidazolium salts as antifungal agents: strong antibiofilm activity against multidrug-resistant Candida tropicalis isolates. Lett Appl Microbiol 60:66–71.  https://doi.org/10.1111/lam.12338 CrossRefGoogle Scholar
  6. Berman HM, Battistuz T, Bhat TN, Bluhm WF, Bourne PE, Burkhardt K, Feng Z, Gilliland GL, Iype L, Jain S, Fagan P, Marvin J, Padilla D, Ravichandran V, Schneider B, Thanki N, Weissig H, Westbrook JD, Zardecki C (2002) The protein data bank. Acta Crystallogr D Biol Crystallogr 58:899–907 PMID: 12037327CrossRefGoogle Scholar
  7. Biovia-discovery-studio (2018). http://accelrys.com/products/collaborative-science/biovia-discovery-studio (Accessed May 2018).
  8. Birnie CR, Malamud D, Schnaare RL (2000) Antimicrobial evaluation of N-alkylbetaines and N-alkyl-N, N-dimethylamine oxides with variations in chain length. Antimicrob Agents Chemother 44:2514–2517.  https://doi.org/10.1128/AAC.44.9.2514-2517.2000 CrossRefGoogle Scholar
  9. Bodor N, Kaminski JJ, Selk S (1980) Soft drugs. 1. Labile quaternary ammonium salts as soft antimicrobials. J Med Chem 23:469–474.  https://doi.org/10.1021/jm00179a001 CrossRefGoogle Scholar
  10. Boethling RS (1994) Environmental aspects of cationic surfactants. In: Cross J, Singer EJ (eds) Cationic surfactans, Surfactants science series, vol 53. Marcel Dekker, New York, pp 95–135Google Scholar
  11. Boethling RS, Sommer E, DiFiore D (2007) Designing small molecules for biodegradability. Chem Rev 107:2207–2227.  https://doi.org/10.1021/cr050952t CrossRefGoogle Scholar
  12. Cetylpyridinium chloride, monohydrate (2016). Safety data sheet MSDS005. https://www.vertellus.com/Documents/msds/Cetylpyridinium%20Chloride%20Monohydrate%20(CPC)%20English.pdf. Accessed 20 June 2016
  13. Cornellas A, Perez L, Comelles F, Ribosa I, Manresa A (2011) Self-aggregation and antimicrobial activity of imidazolium and pyridinium based ionic liquids in water solutions. J Colloid Interface Sci 355:164–171.  https://doi.org/10.1016/j.jcis.2010.11.063 CrossRefGoogle Scholar
  14. Couling DJ, Bernot RJ, Docherty KM, Dixon JK, Maginn EJ (2006) Assessing the factors responsible for ionic liquid toxicity to aquatic organisms via quantitative structure-property relationship modelling. Green Chem 8:82–90.  https://doi.org/10.1039/B511333D CrossRefGoogle Scholar
  15. Docherty KM, Dixon JK, Kulpa CF (2007) Biodegradability of imidazolium and pyridinium ionic liquids by an activated sludge microbial community. Biodegradation 18:481–493.  https://doi.org/10.1007/s10532-006-9081-7 CrossRefGoogle Scholar
  16. Elder ST, Preuss A, Schoning K-U, Muhlbauer K (2008) Anti-microbial compositions. US Patent 2008/0070966A1, Assignee: BASF SEGoogle Scholar
  17. Frade RFM, Matias A, Branco LC, CAM A, CMM D (2007) Effect of ionic liquids on human colon carcinoma HT-29 and CaCo-2 cell lines. Green Chem 9:873–877.  https://doi.org/10.1039/B617526K CrossRefGoogle Scholar
  18. Frade RFM, Rosatella AA, Marques CS, Branco LC, Kulkarni PS, NMM M, CAM A, CMM D (2009) Toxicological evaluation on human colon carcinoma cell line (CaCo-2) of ionic liquids based on imidazolium, guanidinium, ammonium, phosphonium, pyridinium and pyrrolidinium cations. Green Chem 11:1660–1665.  https://doi.org/10.1039/B914284N CrossRefGoogle Scholar
  19. Garcia MT, Ribosa I, Perez L, Manresa A, Comelles F (2013) Aggregation behaviour and antimicrobial activity of ester-functionalized imidazolium- and pyridinium-based ionic liquids in aqueous solution. Langmuir 29:2536–2545.  https://doi.org/10.1021/la304752e CrossRefGoogle Scholar
  20. Garcia MT, Ribosa I, Perez L, Manresa A, Comelles F (2014) Self-assembly and antimicrobial activity of long-chain amide-functionalized ionic liquids in aqueous solution. Coll Surf B 123:318–325.  https://doi.org/10.1016/j.colsurfb.2014.09.033 CrossRefGoogle Scholar
  21. Gathergood N, Garsia MT, Scammels PJ (2004) Biodegradable ionic liquids: Part I. Concept, preliminary targets and evaluation. Green Chem 6:166–175.  https://doi.org/10.1039/B315270G CrossRefGoogle Scholar
  22. Gilbert P, Moore LE (2005) Cationic antiseptics: diversity of action under a common epithet. J Appl Microbiol 99:703–715.  https://doi.org/10.1111/j.1365-2672.2005.02664.x CrossRefGoogle Scholar
  23. Gilmore BF, Earle MJ (2011) Development of ionic liquid biocides against microbial biofilm. Chimica Oggi/Chemistry Today 29:50–53Google Scholar
  24. Grabińska-Sota E, Kalka J (2003) An assessment of the toxicity of pyridinium chlorides and their biodegradation intermediates. Environ Int 28:687–690.  https://doi.org/10.1016/S0160-4120(02)00112-5 CrossRefGoogle Scholar
  25. Hancock REW, Sahl H-G (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24:1551–1557.  https://doi.org/10.1038/nbt1267 CrossRefGoogle Scholar
  26. Harjani JR, Singer RD, Garsia MT, Scammels PJ (2008) The design and synthesis of biodegradable pyridinium ionic liquids. Green Chem 10:436–438.  https://doi.org/10.1039/B800534F CrossRefGoogle Scholar
  27. Hartmann DO, Pereira CS (2013) A molecular analysis of the toxicity of alkyltributylphosphonium chlorides in Aspergillus nidulans. New J Chem 37:1569–1577.  https://doi.org/10.1039/C3NJ00167A CrossRefGoogle Scholar
  28. Hodyna D, Bardeau J-F, Metelytsia L, Riabov S, Kobrina L, Laptiy S, Kalashnikova L, Parkhomenko V, Tarasyuk O, Rogalsky S (2016) Efficient antimicrobial activity and reduced toxicity of 1-dodecyl-3-methylimidazolium tetrafluoroborate ionic liquid/β-cyclodextrin complex. Chem Eng J 284:1136–1145.  https://doi.org/10.1016/j.cej.2015.09.041 CrossRefGoogle Scholar
  29. Ivancović T, Hrenović J (2010) Surfactants in the environment. Arh Hig Rada Toksikol 61:95–110.  https://doi.org/10.2478/10004-1254-61-2010-1943 Google Scholar
  30. Jordan A, Cathergood N (2015) Biodegradation of ionic liquids – a critical review. Chem Soc Rev 44:8200–8237.  https://doi.org/10.1039/C5CS00444F CrossRefGoogle Scholar
  31. Kanjilal S, Sunitha S, Reddy PS, Kumar KP, Murty USN, Prasad RBN (2009) Synthesis and evaluation of micellar properties and antimicrobial activities of imidazole-based surfactants. Eur J Lipid Sci Technol 111:941–948.  https://doi.org/10.1002/ejlt.200800292 CrossRefGoogle Scholar
  32. Kawasaki K, Masubuchi M, Morikami K, Sogabe S, Aoyama T, Ebiike H, Niizuma S, Hayase M, Fujii T, Sakata K, Shindoh H, Shiratori Y, Aoki Y, Ohtsuka T, Shimma N (2003) Design and synthesis of novel benzofurans as a new class of antifungal agents targeting fungal N-myristoyltransferase. Part 3. Bioorg Med Chem Lett 13:87–91.  https://doi.org/10.1016/S0960-894X(02)00844-2 CrossRefGoogle Scholar
  33. Kopecky F (1996) Micellization and other associations of amphiphilic antimicrobial quaternary ammonium salts in aqueous solutions. Pharmazie 51:135–144 PMID: 8900863Google Scholar
  34. Kumar RA, Papaїconomou N, Lee JM, Salminen J, Clark DS, Prausnitz JM (2009) In vitro cytotoxicities of ionic liquids: effect of cation rings, functional groups, and anions. Environ Toxicol 24(4):388–395.  https://doi.org/10.1002/tox.20443 CrossRefGoogle Scholar
  35. Łuczak J, Jungnickel C, Łacka I, Stolte S, Hupka J (2010) Antimicrobial and surface activity of 1-alkyl-3-methylimidazolium derivatives. Green Chem 12:593–601.  https://doi.org/10.1039/B921805J CrossRefGoogle Scholar
  36. Malik MA, Hashim MA, Nabi F, Al-Thabaiti SA, Khan Z (2011) Anti-corrosion ability of surfactants: a review. Int J Electrochem Sci 6:1927–1948Google Scholar
  37. Marvin (2018). http://www.chemaxon.com/products/marvin/marvinsketch (Accessed May 2018).
  38. Mazu TK, Bricker BA, Flores-Rozas H, Ablordeppey SY (2016) The mechanistic targets of antifungal agents: an overview. Mini Rew Med Chem 16:555–578 PMID: 26776224 CrossRefGoogle Scholar
  39. Mishra S, Tyagi VK (2007) Esterquats: the novel class of cationic fabric softeners. J Oleo Sci 56:269–276 PMID: 17898491CrossRefGoogle Scholar
  40. MOPAC2016 (2016) Stewart JJP. Stewart Computational Chemistry, Colorado Springs http://openmopac.net/MOPAC2016.html
  41. Morais DS, Guedes RM, Lopes MA (2016) Antimicrobial approaches for textiles: from research to market. Dent Mater 9:E498.  https://doi.org/10.3390/ma9060498 Google Scholar
  42. Morris JM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 30:2785–2791.  https://doi.org/10.1002/jcc.21256 CrossRefGoogle Scholar
  43. OECD Guideline for testing of chemicals (1992) Fish, acute toxicity test No 203, p 9Google Scholar
  44. Park CJ, Song SX, Kim DH, Gye MC (2016) Developmental and acute toxicity of cetylpyridinium chloride in Bombina orientalis (Amphibia: Anura). Aquat Toxicol 177:446–453.  https://doi.org/10.1016/j.aquatox.2016.06.022 CrossRefGoogle Scholar
  45. Pernak J, Sobaszkiewicz K, Mirska I (2003) Anti-microbial activities of ionic liquids. Green Chem 5:52–56.  https://doi.org/10.1039/B207543C CrossRefGoogle Scholar
  46. Petrocci AN (1983) Surface active agents: quaternary ammonium compounds. In: Block SS (ed) Disinfection, sterilization and preservation. Lea & Febiger Pub, Philadelphia, pp 309–329Google Scholar
  47. Pretti C, Chiappe C, Baldetti I, Brunini S, Monni G, Intorre L (2009) Acute toxicity of ionic liquids for three freshwater organisms: Pseudokirchneriella subcapitata. Daphnia magna and Danio rerio Ecotoxicol Environ Saf 72:1170–1176.  https://doi.org/10.1016/j.ecoenv.2008.09.010 CrossRefGoogle Scholar
  48. Przestalski S, Sarapuk J, Kleszczyńska H, Gabrielska J, Hładyszowski J, Trela Z, Kuczera J (2000) Influence of amphiphilic compounds on membranes. Acta Biochim Pol 47:627–638 PMID: 11310965Google Scholar
  49. Puchta R, Krings P, Sandkuehler P (1993) A new generation of softeners. Tenside Surfactant Deterg 30(3):186–191Google Scholar
  50. Ranke J, Mölter K, Stock F, Bottin-Weber U, Poczobutt J, Hoffmann J, Ondruschka B, Filser J, Jastorff B (2004) Biological effects of imidazolium ionic liquids with varying chain lengths in acute Vibrio fischeri and WST-1 cell viability assays. Ecotoxicol Environ Saf 58:396–404.  https://doi.org/10.1016/S0147-6513(03)00105-2 CrossRefGoogle Scholar
  51. Sanner MF (1999) Python: a programming language for software integration and development. J Mol Graph Model 17:57–61 PMID: 10660911Google Scholar
  52. Schrekker HS, Donato RK, Fuentefria AM, Bergamo V, Oliveira LF, Machado MM (2013) Imidazolium salts as antifungal agents: activity against emerging yeast pathogens, without human leucocyte toxicity. Med Chem Commun 4:1457–1460.  https://doi.org/10.1039/C3MD00222E CrossRefGoogle Scholar
  53. Składanowski AC, Stepnowski P, Kleszczyński K, Dmochowska B (2005) AMP deaminase in vitro inhibition by xenobiotics: a potential molecular method for risk assessment of synthetic nitro- and polycyclic musks, imidazolium ionic liquids and N-glucopyranosyl ammonium salts. Environ Toxicol Pharmacol 19(2):291–296.  https://doi.org/10.1016/j.etap.2004.08.005 CrossRefGoogle Scholar
  54. Sogabe S, Masubuchi M, Sakata K, Fukami TA, Morikami K, Shiratori Y, Ebiike H, Kawasaki K, Aoki Y, Shimma N, D′Arcy A, Winkler FK, Banner DW, Ohtsuka T (2002) Crystal structures of Candida albicans N-myristoyltransferase with two distinct inhibitors. Chem Biol 9:1119–1128.  https://doi.org/10.1016/S1074-5521(02)00240-5 CrossRefGoogle Scholar
  55. Sreevidya VS, Lenz KA, Svoboda KR, Ma H (2018) Benzalkonium chloride, benzethonium chloride, and chloroxylenol – three replacement antimicrobials are more toxic than triclosan and triclocarban in two model organisms. Environ Pollut 235:814–824.  https://doi.org/10.1016/j.envpol.2017.12.108 CrossRefGoogle Scholar
  56. Stock F, Hoffmann J, Ranke J, Störmann R, Ondruschka B, Jastorff B (2004) Effects of ionic liquids on the acetylcholinesterase – a structure–activity relationship consideration. Green Chem 6:286–290.  https://doi.org/10.1039/B402348J CrossRefGoogle Scholar
  57. Stolte S, Arning J, Bottin-Weber U, Müller A, Pitner W-R, Welz-Biermann U, Jastorff B, Ranke J (2007) Effects of different head groups and functionalised side chains on the cytotoxicity of ionic liquids. Green Chem 9:760–767.  https://doi.org/10.1039/B711119C CrossRefGoogle Scholar
  58. Stolte S, Steudte S, Igartua A, Stepnowski P (2011) The biodegradation of ionic liquids – the view from a chemical structure perspective. Curr Org Chem 15:1946–1973.  https://doi.org/10.2174/138527211795703603 CrossRefGoogle Scholar
  59. Tee KL, Roccatano D, Stolte S, Arning J, Jastorff B, Schwaneberg U (2008) Ionic liquid effects on the activity of monooxygenase P450 BM-3. Green Chem 10:117–123.  https://doi.org/10.1039/B714674D CrossRefGoogle Scholar
  60. Tischer M, Pradel G, Ohlsen K, Holzgrabe U (2012) Quaternary ammonium salts and their antimicrobial potential: targets or nonspecific interactions? Chem Med Chem 7:22–31.  https://doi.org/10.1002/cmdc.201100404 CrossRefGoogle Scholar
  61. Trindade JR, Visak ZP, Blesic M, Marrucho IM, Coutinho JAP, Canongia Lopes JN, Rebelo LPN (2007) Salting-out effects inaqueous ionic liquid solutions: cloud-point temperature shifts. J Phys Chem B 111:4737–4741.  https://doi.org/10.1021/jp067022d CrossRefGoogle Scholar
  62. Venkata Nancharaiah Y, Reddy GK, Lalithamanasa P, Venugopalan VP (2012) The ionic liquid 1-alkyl-3-methylimidazolium demonstrates comparable antimicrobial and antibiofilm behavior to a cationic surfactant. Biofouling 28:1141–1149.  https://doi.org/10.1080/08927014.2012.736966 CrossRefGoogle Scholar
  63. Walker EB (2003) Quaternary ammonium compounds. In: Paulson D (ed) Handbook of topical antimicrobials: industrial applications in consumer products and pharmaceuticals. Marcel Dekker, New York, pp 99–116Google Scholar
  64. Wang X, Ohlin CA, Lu Q, Fei Z, Hu J, Dyson PJ (2007) Cytotoxicity of ionic liquids and precursor compounds towards human cell line HeLa. Green Chem 9:1191–1197.  https://doi.org/10.1039/B704503D CrossRefGoogle Scholar
  65. Wells AS, Coombe VT (2006) On the freshwater ecotoxicity and biodegradation properties of some common ionic liquids. Org Process Res Dev 10:794–798.  https://doi.org/10.1021/op060048i CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Maria Trush
    • 1
  • Larysa Metelytsia
    • 1
  • Ivan Semenyuta
    • 1
  • Larysa Kalashnikova
    • 1
  • Oleksiy Papeykin
    • 1
  • Irina Venger
    • 1
  • Oksana Tarasyuk
    • 1
  • Larysa Bodachivska
    • 1
  • Volodymyr Blagodatnyi
    • 2
  • Sergiy Rogalsky
    • 1
    Email author
  1. 1.V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of National Academy of Science of UkraineKyivUkraine
  2. 2.Shupyk National Medical Academy of Postgraduate EducationKyivUkraine

Personalised recommendations

Cite article

Buy options