Abstract
The goal of this study was to investigate the effect of the environmental conditions such as the temperature change, incubation time and surface type on the resistance of Staphylococcus aureus biofilms to disinfectants. The antibiofilm assays were performed against biofilms grown at 20 °C, 30 °C and 37 °C, on the stainless steel and polycarbonate, during 24 and 48 h. The involvement of the biofilm matrix and the bacterial membrane fluidity in the resistance of sessile cells were investigated. Our results show that the efficiency of disinfectants was dependent on the growth temperature, the surface type and the disinfectant product. The increase of growth temperature from 20 °C to 37 °C, with an incubation time of 24 h, increased the resistance of biofilms to cationic antimicrobials. This change of growth temperature did not affect the major content of the biofilm matrix, but it decreased the membrane fluidity of sessile cells through the increase of the anteiso-C19 relative amount. The increase of the biofilm resistance to disinfectants, with the rise of the incubation time, was dependent on both growth temperature and disinfectant product. The increase of the biofilm age also promoted increases in the matrix production and the membrane fluidity of sessile cells. The resistance of S. aureus biofilm seems to depend on the environment of the biofilm formation and involves both extracellular matrix and membrane fluidity of sessile cells. Our study represents the first report describing the impact of environmental conditions on the matrix production, sessile cells membrane fluidity and resistance of S. aureus biofilms to disinfectants.
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Alvarez-Ordonez A, Fernandez A, Lopez M, Arenas R, Bernardo A (2008) Modifications in membrane fatty acid composition of Salmonella typhimurium in response to growth conditions and their effect on heat resistance. Int J Food Microbiol 123(3):212–219. doi:10.1016/j.ijfoodmicro.2008.01.015
Arad E, Navon-Venezia S, Gur E, Kuzmenko B, Glick R, Frenkiel-Krispin D, Kramer E, Carmeli Y, Barnea Y (2013) Novel rat model of methicillin-resistant Staphylococcus aureus-infected silicone breast implants: a study of biofilm pathogenesis. Plast Reconstr Surg 131(2):205–214. doi:10.1097/PRS.0b013e3182778590
Arce Miranda JE, Sotomayor CE, Albesa I, Paraje MG (2011) Oxidative and nitrosative stress in Staphylococcus aureus biofilm. FEMS Microbiol Lett 315(1):23–29. doi:10.1111/j.1574-6968.2010.02164.x
Bae YM, Baek SY, Lee SY (2012) Resistance of pathogenic bacteria on the surface of stainless steel depending on attachment form and efficacy of chemical sanitizers. Int J Food Microbiol 153(3):465–473. doi:10.1016/j.ijfoodmicro.2011.12.017
Belessi CE, Gounadaki AS, Psomas AN, Skandamis PN (2011) Efficiency of different sanitation methods on Listeria monocytogenes biofilms formed under various environmental conditions. Int J Food Microbiol 1(145):25. doi:10.1016/j.ijfoodmicro.2010.10.020
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F (2011a) Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27(9):1017–1032. doi:10.1080/08927014.2011.626899
Bridier A, Dubois-Brissonnet F, Greub G, Thomas V, Briandet R (2011b) Dynamics of the action of biocides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 55(6):2648–2654. doi:10.1128/AAC.01760-10
Brooks JD, Flint SH (2008) Biofilms in the food industry: problems and potential solutions. Int J Food Sci Technol 43(12):2163–2176. doi:10.1111/j.1365-2621.2008.01839.x
Campanac C, Pineau L, Payard A, Baziard-Mouysset G, Roques C (2002) Interactions between biocide cationic agents and bacterial biofilms. Antimicrob Agents Chemother 46(5):1469–1474. doi:10.1128/AAC.46.5.1469-1474.2002
Carpentier B, Cerf O (1993) Biofilms and their consequences, with particular reference to hygiene in the food industry. J Appl Bacteriol 75(6):499–511. doi:10.1111/j.1365-2672.1993.tb01587.x
Chaturongkasumrit Y, Takahashi H, Keeratipibul S, Kuda T, Kimura B (2011) The effect of polyesterurethane belt surface roughness on Listeria monocytogenes biofilm formation and its cleaning efficiency. Food Control 22(12):1893–1899. doi:10.1016/j.foodcont.2011.04.032
Chavant P, Gaillard-Martinie B, Hebraud M (2004) Antimicrobial effects of sanitizers against planktonic and sessile Listeria monocytogenes cells according to the growth phase. FEMS Microbiol Lett 236(2):241–248. doi:10.1111/j.1574-6968.2004.tb09653.x
Chihib NE, Ribeiro da Silva M, Delattre G, Laroche M, Federighi M (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(1):155–160. doi:10.1111/j.1574-6968.2003.tb11512.x
Chihib NE, Tierny Y, Mary P, Hornez JP (2005) Adaptational changes in cellular fatty acid branching and unsaturation of Aeromonas species as a response to growth temperature and salinity. Int J Food Microbiol 102(1):113–119. doi:10.1016/j.ijfoodmicro.2004.12.005
Choi N-Y, Kim B-R, Bae Y-M, Lee S-Y (2013) Biofilm formation, attachment, and cell hydrophobicity of foodborne pathogens under varied environmental conditions. J Korean Soc Appl Biol Chem 56(2):207–220. doi:10.1007/s13765-012-3253-4
Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284(5418):1318–1322. doi:10.1126/science.284.5418.1318
Crago B, Ferrato C, Drews SJ, Svenson LW, Tyrrell G, Louie M (2012) Prevalence of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in food samples associated with foodborne illness in Alberta, Canada from 2007 to 2010. Food Microbiol 32(1):202–205. doi:10.1016/j.fm.2012.04.012
da Silva Meira QG, de Medeiros Barbosa I, Alves Aguiar Athayde AJ, de Siqueira-Júnior JP, de Souza EL (2012) Influence of temperature and surface kind on biofilm formation by Staphylococcus aureus from food-contact surfaces and sensitivity to sanitizers. Food Control 25(2):469–475. doi:10.1016/j.foodcont.2011.11.030
Davison WM, Pitts B, Stewart PS (2010) Spatial and temporal patterns of biocide action against Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 54(7):2920–2927. doi:10.1128/AAC.01734-09
Denich TJ, Beaudette LA, Lee H, Trevors JT (2003) Effect of selected environmental and physico-chemical factors on bacterial cytoplasmic membranes. J Microbiol Methods 52(2):149–182. doi:10.1016/S0167-7012(02)00155-0
Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8(9):881–890
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356. doi:10.1021/ac60111a017
Dubois-Brissonnet F, Naitali M, Mafu AA, Briandet R (2011) Induction of fatty acid composition modifications and tolerance to biocides in Salmonella enterica serovar Typhimurium by plant-derived terpenes. Appl Environ Microbiol 77(3):906–910. doi:10.1128/AEM.01480-10
Gilbert P, Moore LE (2005) Cationic antiseptics: diversity of action under a common epithet. J Appl Microbiol 99(4):703–715. doi:10.1111/j.1365-2672.2005.02664.x
Gounadaki AS, Skandamis PN, Drosinos EH, Nychas GJ (2008) Microbial ecology of food contact surfaces and products of small-scale facilities producing traditional sausages. Food Microbiol 25(2):313–323. doi:10.1016/j.fm.2007.10.001
Gutierrez D, Delgado S, Vazquez-Sanchez D, Martinez B, Cabo ML, Rodriguez A, Herrera JJ, Garcia P (2012) Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Appl Environ Microbiol 78(24):8547–8554. doi:10.1128/AEM.02045-12
Herrera JJ, Cabo ML, Gonzalez A, Pazos I, Pastoriza L (2007) Adhesion and detachment kinetics of several strains of Staphylococcus aureus subsp. aureus under three different experimental conditions. Food Microbiol 24(6):585–591. doi:10.1016/j.fm.2007.01.001
Jenkinson HF, Lappin-Scott HM (2001) Biofilms adhere to stay. Trends Microbiol 9(1):9–10. doi:10.1016/S0966-842X(00)01891-6
Joseph B, Otta SK, Karunasagar I (2001) Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int J Food Microbiol 64(3):367–372. doi:10.1016/S0168-1605(00)00466-9
Kaneda T (1991) Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev 55(2):288–302
Kerouanton A, Hennekinne JA, Letertre C, Petit L, Chesneau O, Brisabois A, De Buyser ML (2007) Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol 115(3):369–375. doi:10.1016/j.ijfoodmicro.2006.10.050
Marques SC, Rezende JGOS, Alves LAF, Silva BC, Alves E, Abreu LR, Piccoli RH (2007) Formation of biofilms by Staphylococcus aureus on stainless steel and glass surfaces and its resistance to some selected chemical sanitizers. Braz J Microbiol 38:538–543. doi:10.1590/S1517-83822007000300029
Neunlist MR, Federighi M, Laroche M, Sohier D, Delattre G, Jacquet C, Chihib NE (2005) Cellular lipid fatty acid pattern heterogeneity between reference and recent food isolates of Listeria monocytogenes as a response to cold stress. Antonie Van Leeuwenhoek 88(3–4):199–206. doi:10.1007/s10482-005-5412-7
Nguyen HDN, Yuk H-G (2013) Changes in resistance of Salmonella Typhimurium biofilms formed under various conditions to industrial sanitizers. Food Control 29(1):236–240. doi:10.1016/j.foodcont.2012.06.006
Normanno G, La Salandra G, Dambrosio A, Quaglia NC, Corrente M, Parisi A, Santagada G, Firinu A, Crisetti E, Celano GV (2007) Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. Int J Food Microbiol 115(3):290–296. doi:10.1016/j.ijfoodmicro.2006.10.049
Pagedar A, Singh J, Batish VK (2010) Surface hydrophobicity, nutritional contents affect Staphylococcus aureus biofilms and temperature influences its survival in preformed biofilms. J Basic Microbiol 50(1):201000034. doi:10.1002/jobm.201000034
Poulsen LV (1999) Microbial Biofilm in food processing. LWT-Food Sci Technol 32(6):321–326. doi:10.1006/fstl.1999.0561
Rode TM, Langsrud S, Holck A, Moretro T (2007) Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int J Food Microbiol 116(3):372–383. doi:10.1016/j.ijfoodmicro.2007.02.017
Schlisselberg DB, Yaron S (2013) The effects of stainless steel finish on Salmonella Typhimurium attachment, biofilm formation and sensitivity to chlorine. Food Microbiol 35(1):65–72. doi:10.1016/j.fm.2013.02.005
Simões M, Simões LC, Vieira MJ (2010) A review of current and emergent biofilm control strategies. LWT-Food Sci Technol 43(4):573–583. doi:10.1016/j.lwt.2009.12.008
Singh VK, Hattangady DS, Giotis ES, Singh AK, Chamberlain NR, Stuart MK, Wilkinson BJ (2008) Insertional inactivation of branched-chain alpha-keto acid dehydrogenase in Staphylococcus aureus leads to decreased branched-chain membrane fatty acid content and increased susceptibility to certain stresses. Appl Environ Microbiol 74(19):5882–5890. doi:10.1128/AEM.00882-08
Singh AV, Vyas V, Patil R, Sharma V, Scopelliti PE, Bongiorno G, Podesta A, Lenardi C, Gade WN, Milani P (2011) Quantitative characterization of the influence of the nanoscale morphology of nanostructured surfaces on bacterial adhesion and biofilm formation. PLoS One 6(9):26. doi:10.1371/journal.pone.0025029
Song L, Wu J, Xi C (2012) Biofilms on environmental surfaces: evaluation of the disinfection efficacy of a novel steam vapor system. Am J Infect Control 40(10):926–930. doi:10.1016/j.ajic.2011.11.013
Srinivasan A, Wolfenden LL, Song X, Mackie K, Hartsell TL, Jones HD, Diette GB, Orens JB, Yung RC, Ross TL, Merz W, Scheel PJ, Haponik EF, Perl TM (2003) An outbreak of Pseudomonas aeruginosa infections associated with flexible bronchoscopes. N Engl J Med 348(3):221–227. doi:10.1056/NEJMoa021808
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(11):5258–5264. doi:10.1128/AEM.68.11.5258-5264.2002
Tote K, Horemans T, Vanden Berghe D, Maes L, Cos P (2010) Inhibitory effect of biocides on the viable masses and matrices of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 76(10):3135–3142. doi:10.1128/AEM.02095-09
Vazquez-Sanchez D, Habimana O, Holck A (2013) Impact of food-related environmental factors on the adherence and biofilm formation of natural Staphylococcus aureus isolates. Curr Microbiol 66(2):110–121. doi:10.1007/s00284-012-0247-8
Warnke PH, Becker ST, Podschun R, Sivananthan S, Springer IN, Russo PA, Wiltfang J, Fickenscher H, Sherry E (2009) The battle against multi-resistant strains: renaissance of antimicrobial essential oils as a promising force to fight hospital-acquired infections. J Craniomaxillofac Surg 37(7):392–397. doi:10.1016/j.jcms.2009.03.017
Zhang YM, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6(3):222–233. doi:10.1038/nrmicro1839
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The authors are grateful to the French Agency for Research and Technology (ANRT) and SCIENTIS laboratory for the CIFRE grant supporting this work (CIFRE: 2010/0205).
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Abdallah, M., Chataigne, G., Ferreira-Theret, P. et al. Effect of growth temperature, surface type and incubation time on the resistance of Staphylococcus aureus biofilms to disinfectants. Appl Microbiol Biotechnol 98, 2597–2607 (2014). https://doi.org/10.1007/s00253-013-5479-4
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DOI: https://doi.org/10.1007/s00253-013-5479-4