Abstract
The present work aimed at studying physiological properties of Pseudomonas aeruginosa cells actively detached from biofilm formed on stainless steel and comparing them with their planktonic counterparts as a function of growth temperature (20 °C and 37 °C). The susceptibility of P. aeruginosa cells to benzalkonium chloride (BAC) was studied. Furthermore, the effect of BAC on the cell membrane integrity and the role of the cell membrane fluidity in the cell-scale-resistance mechanism were investigated. Our results showed that actively detached biofilm cells were more susceptible to BAC treatment than planktonic ones. A greater leakage of intracellular potassium after BAC addition was observed in actively detached biofilm cells, which reflects their membrane vulnerability. The rise of the growth temperature from 20 to 37 °C increased the membrane rigidity of planktonic cells comparatively to their actively detached biofilm ones. Under experimental conditions developed in this work, our data highlighted that actively biofilm-detached and planktonic P. aeruginosa cells have distinguishable phenotypes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdallah M, Chataigne G, Ferreira-Theret P et al (2014) Effect of growth temperature, surface type and incubation time on the resistance of Staphylococcus aureus biofilms to disinfectants. Appl Microbiol Biotechnol. https://doi.org/10.1007/s00253-013-5479-4
Abdallah M, Benoliel C, Ferreira-Theret P et al (2015a) Effect of culture conditions on the resistance of Pseudomonas aeruginosa biofilms to disinfecting agents. Biofouling 31:49–59. https://doi.org/10.1080/08927014.2014.993390
Abdallah M, Khelissa O, Ibrahim A et al (2015b) Impact of growth temperature and surface type on the resistance of Pseudomonas aeruginosa and Staphylococcus aureus biofilms to disinfectants. Int J Food Microbiol 214:38–47. https://doi.org/10.1016/j.ijfoodmicro.2015.07.022
Allison DG, Evans DJ, Brown MR, Gilbert P (1990) Possible involvement of the division cycle in dispersal of Escherichia coli from biofilms. J Bacterial 172:1667–1669
Bester E, Wolfaardt G, Joubert L et al (2005) Planktonic-cell yield of a Pseudomonad biofilm. Appl Environ Microbiol 71:7792–7798. https://doi.org/10.1128/AEM.71.12.7792-7798.2005
Brooun A, Liu S, Lewis K (2000) A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 44:640–646
Brown JL, Ross T, McMeekin TA, Nichols PD (1997) Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. Int J Food Microbiol 37:163–173. https://doi.org/10.1016/S0168-1605(97)00068-8
Chihib N-E, Ribeiro da Silva M, Delattre G et al (2003) Different cellular fatty acid pattern behaviours of two strains of Listeria monocytogenes Scott A and CNL 895807 under different temperature and salinity conditions. FEMS Microbiol Lett 218:155–160. https://doi.org/10.1111/j.1574-6968.2003.tb11512.x
Davey ME, O’toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867
Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2:114–122. https://doi.org/10.1038/nrd1008
Dunne WM (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15:155–166. https://doi.org/10.1128/CMR.15.2.155-166.2002
Elsen S, Huber P, Bouillot S et al (2014) A type III secretion negative clinical strain of Pseudomonas aeruginosa employs a two-partner secreted exolysin to induce Hemorrhagic Pneumonia. Cell Host Microbe 15:164–176. https://doi.org/10.1016/j.chom.2014.01.003
Emiola A, Andrews SS, Heller C, George J (2016) Crosstalk between the lipopolysaccharide and phospholipid pathways during outer membrane biogenesis in Escherichia coli. Proc Natl Acad Sci USA 113:3108–3113. https://doi.org/10.1073/pnas.1521168113
Gerba CP (2015) Quaternary ammonium biocides: efficacy in application. Appl Environ Microbiol 81:464–469. https://doi.org/10.1128/AEM.02633-14
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
Jefferson KK (2004) What drives bacteria to produce a biofilm? FEMS Microbiol Lett 236:163. https://doi.org/10.1111/j.1574-6968.2004.tb09643.x
Johnston MD, Hanlon GW, Denyer SP, Lambert RJW (2003) Membrane damage to bacteria caused by single and combined biocides. J Appl Microbiol 94:1015–1023
Kaplan J (2010) Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J Dent Res 89:205–218. https://doi.org/10.1177/0022034509359403
Maillard J-Y (2002) Bacterial target sites for biocide action. J Appl Microbiol 92:16S–27S
Mustapha A, Liewen MB (1989) Destruction of Listeria monocytogenes by sodium hypochlorite and quaternary ammonium sanitizers. J Food Prot 52:306–311. https://doi.org/10.4315/0362-028X-52.5.306
Parsons JB, Rock CO (2013) Bacterial lipids: metabolism and membrane homeostasis. Prog Lipid Res 52:249–276. https://doi.org/10.1016/j.plipres.2013.02.002
Sauer K, Camper AK, Ehrlich GD et al (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184:1140–1154. https://doi.org/10.1128/jb.184.4.1140-1154.2002
Smith K, Hunter IS (2008) Efficacy of common hospital biocides with biofilms of multi-drug resistant clinical isolates. J Med Microbiol 57:966–973. https://doi.org/10.1099/jmm.0.47668-0
To MS, Favrin S, Romanova N, Griffiths MW (2002) Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Appl Environ Microbiol 68:5258–5264
Zhang Y-M, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222–233. https://doi.org/10.1038/nrmicro1839
Acknowledgements
This work was carried out within the ALIBIOTECH framework (Agroalimentaire et Biotechnologie, Nord Pas-de-Calais region) program. The authors also thank the Haut de France region and FEDER (Fonds européen de développement régional) for their financial support.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Human and animal rights statement
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Djamel Drider.
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
Khelissa, S.O., Abdallah, M., Jama, C. et al. Actively detached Pseudomonas aeruginosa biofilm cell susceptibility to benzalkonium chloride and associated resistance mechanism. Arch Microbiol 201, 747–755 (2019). https://doi.org/10.1007/s00203-019-01643-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-019-01643-x