Microorganisms and cationic surfactants
Natalia Kula 1 , Edyta Mazurkiewicz 1 , Ewa Obłąk 1Abstract
Quaternary ammonium salts (QAS) as cationic surfactants with an amphiphilic structure show biocidal activity against non-pathogenic and pathogenic microorganisms (Gram-positive, Gram-negative bacteria, fungi, as well as lipophilic viruses) occurring in planktonic form or forming biofilms. They can also coat the surface of various materials (glass, metal, silicone, polyester) from which medical devices are made, such as: catheters, implants, heart valves, endoprostheses, and this allows inhibiting the adhesion of microorganisms to these surfaces. In their chemical structure, these surfactants contain labile bonds, e.g. ester or amide bonds, which enable the biodegradation of the compounds. Thanks to this, they are classified as “green chemistry”. Their biological activity depends on the length of the hydrophobic chain and the structure of the hydrophilic head of the compound. QAS have an affinity for the cell membrane by interacting with its lipids and proteins, which can lead to its disintegration. They have the ability to inhibit the activity of H+-ATPase of the cell membrane, the enzyme responsible for its electrochemical gradient and the transport of nutrients to the cell, e.g. amino acids. These compounds can influence the lipid composition (quantitative and qualitative) of the cell membrane of microorganisms. They are also inhibitors of respiratory processes and can induce the formation of reactive oxygen species. These surfactants are capable of forming micelles and liposomes in an aqueous environment. They are widely used in medicine (as disinfectants, DNA carriers in gene therapy), in industry and environmental protection (as biocides, preservatives) and in agriculture (as fungicides). The widespread use of QAS in many fields causes the growing resistance of microorganisms to these compounds. A common mechanism that generates reduced susceptibility to QAS is the presence of efflux pumps.
References
- 1. Agrawal A., Hila A., Tutuian R., Maine I., Castell D.O.: Bethanecholimproves smooth muscle function in patients with severe ineffectiveesophageal motility. J. Clin. Gastroenterol., 2007; 41: 366–370
Google Scholar - 2. Aiad I., El-Sukkary M.M., Soliman E.A., El-Awady M.Y., Shaban S.M.:Characterization, surface properties and biological activity of new preparedcationic surfactants. J. Ind. Eng. Chem., 2014; 20: 1633–1640
Google Scholar - 3. Alam M.S., Takahashi S., Ito M., Komura M., Ono M., Daio C., SangsriratanakulN., Shoham D., Alam J., Takehara K.: Virucidal efficacy ofa quaternary ammonium compound with food additive–grade calciumhydroxide toward avian influenza virus and Newcastle disease virus onabiotic carriers. Avian Dis., 2018; 62: 355–363
Google Scholar - 4. Alav I., Sutton J.M., Rahman K.M.: Role of bacteria efflux pumpsin biofilm formation. J. Antimicrob. Chemother., 2018; 73: 2003–2020
Google Scholar - 5. Andrade Lopes L.A., dos Santos Rodrigues J.B., Magnani M., de SouzaE.L., de Siqueira-Júnior J.P.: Inhibitory effects of flavonoids on biofilmformation by Staphylococcus aureus that overexpresses efflux proteingenes. Microb. Pathog., 2017; 107: 193–197
Google Scholar - 6. Azarmi R., Ashjaran A.: Type and application of some commonsurfactants. J. Chem. Pharm. Res., 2015; 7: 632–640
Google Scholar - 7. Bay D.C., Stremick C.A., Slipski C.J., Turner R.J.: Secondary multidrugefflux pump mutants alter Escherichia coli biofilm growth inthe presence of cationic antimicrobial compounds. Res. Microbiol.,2017; 168: 208–221
Google Scholar - 8. Bell P.C., Bergsma M., Dolbnya I.P., Bras W., Stuart M.C., RowanA.E., Feiters M.C., Engberts J.B.: Transfection mediated by gemini surfactants:Engineered escape from the endosomal compartment. J. Am.Chem. Soc., 2003; 125: 1551–1558
Google Scholar - 9. Biles C.L., Wright D., Fuego M., Guinn A., Cluck T., Young J., MartinM., Biles J., Poudyal, S.: Differential chlorate inhibition of Chaetomiumglobosum germination, hyphal growth, and perithecia synthesis. Mycopathologia,2012; 174: 475–487
Google Scholar - 10. Böcking T., Barrow K.D., Netting A.G., Chilcott T.C., Coster H.G.,Höfer M.: Effects of singlet oxygen on membrane sterols in the yeastSaccharomyces cerevisiae. Eur. J. Biochem., 2000; 267: 1607–1618
Google Scholar - 11. Bozzuto G., Molinari A.: Liposomes as nanomedical devices. Int.J. Nanomedicine, 2015; 10: 975–999
Google Scholar - 12. Brycki B., Szulc A.: Gemini alkyldeoxy-D-glucitolammonium saltsas modern surfactants and microbiocides: Synthesis, antimicrobialand surface activity, biodegradation. PLoS One, 2014; 9: e84936
Google Scholar - 13. Buffet-Bataillon S., Le Jeune A., Le Gall-David S., Bonnaure-MalletM., Jolviet-Gougeon A.: Molecular mechanisms of higher MICs of antibioticsand quaternary ammonium compounds for Escherichia coli isolatedfrom bacteraemia. J. Antimicrob. Chemoth., 2012; 67: 2837–2842
Google Scholar - 14. Buffet-Bataillon S., Tattevin P., Maillard J.Y., Bonnaure-Mallet M.,Jolviet-Gougeon A.: Efflux pump induction by quaternary ammoniumcompounds and fluoroquinolone resistance in bacteria. Future Microbiol.,2016; 11: 81–92
Google Scholar - 15. Campbell R.B., Fukumura D., Brown E.B., Mazzola L.M., Izumi Y.,Jain R.K., Torchilin V.P., Munn L.L.: Cationic charge determines thedistribution of liposomes between the vascular and extravascularcompartments of tumors. Cancer Res., 2002; 62: 6831–6836
Google Scholar - 16. Chou L., Ming K., Chan W.C.: Strategies for the intracellular deliveryof nanoparticles. Chem. Soc. Rev., 2011; 40: 233–245
Google Scholar - 17. Claxton D.P., Jagessar K.L., Steed P.R., Stein R.A., Mchaourab H.S.:Sodium and proton coupling in the conformational cycle of a MATEantiporter from Vibrio cholerae. Proc. Natl. Acad. Sci. USA, 2018; 115:6182–6190
Google Scholar - 18. Costa S.S., Viveiros M., Amaral L., Couto I.: Multidrug efflux pumpsin Staphylococcus aureus: An update. Open Microbiol. J., 2013; 7: 59–71
Google Scholar - 19. Deshpande P., Biswas S., Torchilin V.P.: Current trends in the useof liposomes for tumor targeting. Nanomedicine, 2013; 8: 1509–1528
Google Scholar - 20. Ferreira J.M.: The quat advantage: Quaternary ammonium chlorideand its advantages in healthcare facilities. Perition Dialysis Int.,2015
Google Scholar - 21. Fink J.: General aspects of pipelines. W: Guide to the Practical Useof Chemicals in Refineries and Pipelines, red.: J. Fink. Gulf ProfessionalPublishing, 2016, 3–23
Google Scholar - 22. Fontaine F., Héquet A., Vosin-Chiret A.S., Bouillon A., Lesnard A.,Cresteil T., Jolivalt C., Rault S.: Boronic species as promising inhibitorsof the Staphylococcus aureus NorA efflux pump: Study of 6-substitutedpyridine-3-bronic acid derivatives. Eur. J. Med. Chem., 2015;95: 185–198
Google Scholar - 23. Forbes S., Cowley N., Humphreys G., Mistry H., Amézquita A.,McBain A.J.: Formulation of biocides increases antimicrobial potencyand mitigates the enrichment of nonsusceptible bacteria in multispeciesbiofilms. Appl. Environ. Microbiol., 2017; 83: e03054–16
Google Scholar - 24. Fox E.M., Leonard N., Jordan K.: Physiological and transcriptionalcharacterization of persistent and nonpersistent Listeria monocytogenesisolates. Appl. Environ. Microbiol., 2011; 77: 6559–6569
Google Scholar - 25. Gerba C.P.: Quaternary ammonium biocides: Efficacy in application.Appl. Environ. Microbiol., 2015; 81: 464–469
Google Scholar - 26. Ghatak P.D., Mathew-Steiner S.S., Pandey P., Roy S., Sen C.K.:A surfactant polymer dressing potentiates antimicrobial efficacy inbiofilm disruption. Sci. Rep., 2018; 8: 873
Google Scholar - 27. Ghotaslou R., Yekani M., Memar M.Y.: The role of efflux pumpsin Bacteroides fragilis resistance to antibiotics. Microbiol. Res., 2018;210: 1–5
Google Scholar - 28. Goik U., Załęska-Żyłka I., Pietrzycka A.: Liposomy jako nośnikisubstancji aktywnych przenoszonych w głąb skóry. Inż. Biomater.,2015; 18: 27–39
Google Scholar - 29. Gunawardena G.: Quaternary Ammonium Salt. OChemPal.http://www.ochempal.org/index.php/alphabetical/q-r/quaternaryammonium-salt (08.12.2019)
Google Scholar - 30. Honing G., Martini C.H., Bom A., van Velzen M., Niesters M., AartsL., Dahan A., Boon M.: Safety of sugammadex for reversal of neuromuscularblock. Expert Opin. Drug Saf., 2019; 18: 883–891
Google Scholar - 31. Ito M., Alam M.S., Suzuki M., Takahashi S., Komura M., SangsriratakulN., Shoham D., Takehara K.: Virucidal activity of a quaternaryammonium compound associated with calcium hydroxide on avianinfluenza virus, Newcastle disease virus and infectious bursal diseasevirus. J. Vet. Med. Sci., 2018; 80: 574–577
Google Scholar - 32. Jarmuła A., Obłąk E., Wawrzycka D., Gutowicz J.: Oporność wielolekowazwiązana z aktywnym usuwaniem leków z komórek drobnoustrojów.Postępy Hig. Med. Dośw., 2011; 65: 216–227
Google Scholar - 33. Kampf G.: Biocidal agents used for disinfection can enhance antibioticresistance in gram-negative species. Antibiotics, 2018; 7: 110
Google Scholar - 34. Kosmowska N., Łuczak W., Gwiazdowska D., Michocka K., WieczorekD.: Antibacterial activity of chemical compounds used as surfactants. W:Current Trends in Commodity Science: Development and Assessment ofNon-Food Products, red.: K. Michocka, M. Tichoniuk. Poznań Universityof Economics and Business, Poznań 2016, 54–67
Google Scholar - 35. Krah A., Zachariae U.: Insights into the ion-coupling mechanism inthe MATE transporter NorM-VC. Phys. Biol., 2017; 14: 045009
Google Scholar - 36. Krzyżewska E., Książczyk M., Kędziora A., Futoma-Kołoch B., Bugla-Płoskońska G.: Modyfikacje struktur komórkowych mikroorganizmówwywołane działaniem biocydów. Post. Mikrobiol., 2015; 54: 380–391
Google Scholar - 37. Lipińska-Ojrzanowska A., Walusiak-Skorupa J.: Czwartorzędowezwiązki amoniowe – nowe zagrożenie w środowisku pracy. Med. Pr.,2014; 65: 675–682
Google Scholar - 38. Martínez-Suárez J.V., Ortiz S., López-Alonso V.: Potential impactof the resistance to quaternary ammonium disinfectants on the persistenceof Listeria monocytogenes in food processing environments.Front. Microbiol., 2016; 7: 638
Google Scholar - 39. McNeil H.E., Alav I., Torres R.C., Rossiter A.E., Laycock E., Legood S.,Kaur I., Davies M., Wand M., Webber M.A., Bavro V.N., Blair J.M.: Identificationof binding residues between periplasmic adapter protein (PAP)and RND efflux pumps explains PAP-pump promiscuity and roles inantimicrobial resistance. PLoS Pathog., 2019; 15: e1008101
Google Scholar - 40. Muthuprasanna P., Surya K., Sobhita P., Satish babu I.A., SarathChandiran I., Ganesan A., Shalini S.: Basics and potential applicationsof surfactants – A review. Int. J. Pharm. Tech. Res., 2009; 1: 1354–1365
Google Scholar - 41. Myers D.: Surfactants science and technology, Third edition. Wiley-Interscience A John Wiley & Sons, Inc. Publication, Hoboken, New Jersey2006
Google Scholar - 42. Nagashima S., Matsushima Y., Hamaguchi H., Nagata H., Kontani T.,Moritomo A., Koshika T., Takeuchi M.: Novel quinuclidinyl heteroarylcarbamatederivatives as muscarinic receptor antagonists. Bioorg. Med.Chem., 2014; 22: 3478–3487
Google Scholar - 43. Obłąk E., Bącal J., Lachowicz T.M.: A quaternary ammonium saltas an inhibitor of plasma membrane H+-ATPase in yeast Saccharomycescerevisiae. Cell. Mol. Biol. Lett., 2000; 5: 315–324
Google Scholar - 44. Obłąk E., Gamian A.: Biologiczna aktywność czwartorzędowych soliamoniowych (CSA). Postępy Hig. Med. Dośw., 2010; 64: 201–211
Google Scholar - 45. Obłąk E., Piecuch A., Maciaszczyk-Dziubińska E., Wawrzycka D.:Quaternary ammonium salt N-(dodecyloxycarboxymethyl)-N,N,Ntrimethylammonium chloride induced alterations in Saccharomycescerevisiae physiology. J. Biosci., 2016; 41: 601–614
Google Scholar - 46. Obłąk E., Piecuch A., Rewak-Soroczyńska J., Paluch E.: Activity ofgemini quaternary ammonium salts against microorganisms. Appl.Microbiol. Biotechnol., 2019; 103: 625–632
Google Scholar - 47. Paluch E.: Biologiczna aktywność nowo zsyntezowanych kationowychsurfaktantów wielofunkcyjnych wobec wybranych mikroorganizmów.Praca doktorska. Uniwersytet Wrocławski, Wydział Nauk Biologicznych,Wrocław 2018
Google Scholar - 48. Paluch E., Piecuch A., Obłąk E., Lamch Ł., Wilk K.A.: Antifungal activityof newly synthesized chemodegradable dicephalic-type cationicsurfactants. Colloids Surf. Biointerfaces, 2018; 164: 34–41
Google Scholar - 49. Percival S.L., Mayer D., Salisbury A.M.: Efficacy of a surfactantbasedwound dressing on biofilm control. Wound Repair Regen., 2017;25: 767–773
Google Scholar - 50. Pereira M.O., Machado I., Simões M., Vieira M.J.: Preventing biofilmformation using surfactants. BiofilmClub, Manchester 2007
Google Scholar - 51. Pernak J., Rzemieniecki T., Materna K.: O cieczach jonowych„w pigułce” (historia, właściwości i rozwój). Chemik, 2016; 70: 471–480
Google Scholar - 52. Piskorska T. Obłąk E.: Surfaktanty gemini jako nośniki genów.Postępy Hig. Med. Dośw., 2010; 64: 161–166
Google Scholar - 53. Priyanto S., Mansoori G.A., Suwon A.: Measurement of propertyrelationships of nano-structure micelles and coacervates of asphaltenein a pure solvent. Chem. Eng. Sci., 2001; 56: 6933–6939
Google Scholar - 54. Proszowska A., Siódmak T., Marszałt M.P.: Ciecze jonowe – nowemożliwości w syntezie substancji leczniczych. Ann. Acad. Med. Siles.,2012; 66: 59–65
Google Scholar - 55. Radchenko M., Symersky J., Nie R., Lu M.: Structural basis for theblockade of MATE multidrug efflux pumps. Nat. Commun., 2015; 6: 7995
Google Scholar - 56. Sharma R.K.: Surfactants: Basics and versality in food industries.PharmaTutor, 2014; 2: 17–29
Google Scholar - 57. Simoncic B., Tomsic B.: Structures of novel antimicrobial agents fortextiles – A review. Text. Res. J., 2010; 80: 1721–1737
Google Scholar - 58. Slipski C.J., Zhanel G.G., Bay D.C.: Biocide selective TolC-independentefflux pumps in Enterobacteriaceae. J. Membr. Biol., 2018; 251: 15–33
Google Scholar - 59. Telesiński A., Śnioszek M., Biczak R., Pawłowska B.: Zagrożeniaśrodowiskowe i toksykologiczne wynikające ze stosowaniaczwartorzędowych soli amoniowych. Kosmos, 2016; 65: 495–502
Google Scholar - 60. Teper P., Stachurek I.: Oddziaływanie na zdrowie człowiekai środowisko czwartorzędowych amin jako składników środkówdezynfekujących. Zesz. Nauk. WSZOP, 2016; 1: 113–122
Google Scholar - 61. Wiercińska O., Chojecka A., Kanclerski K., Röhm-Rodowald E., JakimiakB.: Znaczenie pomp efflux w wielolekowej oporności gram-ujemnychbakterii. Med. Dośw. Mikrobiol., 2015; 67: 55–62
Google Scholar - 62. Yadav S., Gandham S.K., Panicucci R., Amiji M.M.: Intranasal braindelivery of cationic nanoemulsion-encapsulated TNFα siRNA in preventionof experimental neuroinflammation. Nanomedicine, 2016; 12:987–1002
Google Scholar - 63. Yu Q., Zhang B., Ma F., Jia C., Xiao C., Zhang B., Xing L., Li M.: Novelmechanisms of surfactants against Candida albicans growth and morphogenesis.Chem. Biol. Interact., 2015; 227: 1–6
Google Scholar - 64. Yuan C.L., Xu Z.Z., Fan M.X., Liu H.Y., Xie Y.H., Zhu T.: Study oncharacteristics and harm of surfactans. J. Chem. Pharm. Res., 2014; 6:2233–2237
Google Scholar - 65. Zied D.C., Nunes J.S., Nicolini V.F., Gimenez A.P., Rinker D.L., Dias E.S.:Tolerance to Lecanicillium fungola and yield of Agaricus bisporus strainsused in Brazil. Sci. Hortic., 2015; 190: 117–122
Google Scholar - 66. Zimmermann S., Klinger-Strobel M., Bohnert J.A., Wendler S.,Rödel J., Pletz M.W., Löffler B., Tuchscherr L.: Clinically approveddrugs inhibit the Staphylococcus aureus multidrug NorA efflux pumpand reduce biofilm formation. Front. Microbiol., 2019; 10: 2762
Google Scholar