Formation of Staphylococcus aureus Biofilm in the Presence of Sublethal Concentrations of Disinfectants Studied via a Transcriptomic Analysis Using Transcriptome Sequencing (RNA-seq)
Language English Country United States Media electronic-print
Document type Journal Article
PubMed
29030437
PubMed Central
PMC5717214
DOI
10.1128/aem.01643-17
PII: AEM.01643-17
Knihovny.cz E-resources
- Keywords
- bacterial decontamination, biofilm formation, gene expression,
- MeSH
- Biofilms drug effects MeSH
- Chloramines pharmacology MeSH
- Disinfectants pharmacology MeSH
- Ethanol pharmacology MeSH
- Sequence Analysis, RNA MeSH
- Gene Expression Profiling MeSH
- Staphylococcus aureus drug effects genetics physiology MeSH
- Transcriptome * MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- chloramine MeSH Browser
- Chloramines MeSH
- Disinfectants MeSH
- Ethanol MeSH
Staphylococcus aureus is a common biofilm-forming pathogen. Low doses of disinfectants have previously been reported to promote biofilm formation and to increase virulence. The aim of this study was to use transcriptome sequencing (RNA-seq) analysis to investigate global transcriptional changes in S. aureus in response to sublethal concentrations of the commonly used food industry disinfectants ethanol (EtOH) and chloramine T (ChT) and their combination (EtOH_ChT) in order to better understand the effects of these agents on biofilm formation. Treatment with EtOH and EtOH_ChT resulted in more significantly altered expression profiles than treatment with ChT. Our results revealed that EtOH and EtOH_ChT treatments enhanced the expression of genes responsible for regulation of gene expression (sigB), cell surface factors (clfAB), adhesins (sdrDE), and capsular polysaccharides (cap8EFGL), resulting in more intact biofilm. In addition, in this study we were able to identify the pathways involved in the adaptation of S. aureus to the stress of ChT treatment. Further, EtOH suppressed the effect of ChT on gene expression when these agents were used together at sublethal concentrations. These data show that in the presence of sublethal concentrations of tested disinfectants, S. aureus cells trigger protective mechanisms and try to cope with them.IMPORTANCE So far, the effect of disinfectants is not satisfactorily explained. The presented data will allow a better understanding of the mode of disinfectant action with regard to biofilm formation and the ability of bacteria to survive the treatment. Such an understanding could contribute to the effort to eliminate possible sources of bacteria, making disinfectant application as efficient as possible. Biofilm formation plays significant role in the spread and pathogenesis of bacterial species.
Central European Institute of Technology Masaryk University Brno Czech Republic
National Centre for Biomolecular Research Faculty of Science Masaryk University Brno Czech Republic
See more in PubMed
Mermel LA, Allon M, Bouza E, Flynn P, O'Grady NP, Raad II, Rijnders BJ, Sheretz RJ, Warren DK. 2010. Clinical practice guidelines for the diagnosis and management of intravascular catheter-related infection: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis 49:1–45. doi:10.1086/599376. PubMed DOI PMC
Graveland H, Duim B, van Duijkeren E, Heederik D, Wagenaar JA. 2011. Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int J Med Microbiol 301:630–634. doi:10.1016/j.ijmm.2011.09.004. PubMed DOI
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 32:202–205. doi:10.1016/j.fm.2012.04.012. PubMed DOI
Doulgeraki AI, Di Ciccio P, Ianieri A, Nychas GJE. 2017. Methicillin-resistant food-related Staphylococcus aureus: a review of current knowledge and biofilm formation for future studies and applications. Res Microbiol 168:1–15. doi:10.1016/j.resmic.2016.08.001. PubMed DOI
Gutierrez D, Delgado S, Vazquez-Sanchez D, Martinez B, Cabo ML, Rodriguez A, Herrera JJ, García P. 2012. Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Appl Environ Microbiol 78:8547–8554. doi:10.1128/AEM.02045-12. PubMed DOI PMC
Gotz F. 2002. Staphylococcus and biofilms. Mol Microbiol 43:1367–1378. PubMed
Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F. 2011. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27:1017–1032. doi:10.1080/08927014.2011.626899. PubMed DOI
Halliman DG, Ahearn DG. 2004. Relative susceptibilities to vancomycin and quinupristin-dalfopristin of adhered and planktonic vancomycin-resistant and vancomycin-susceptible coagulase-negative staphylococci. Curr Microbiol 48:214–218. doi:10.1007/s00284-003-4091-8. PubMed DOI
Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298. doi:10.1126/science.280.5361.295. PubMed DOI
Yarwood JM, Bartels DJ, Volper EM, Greenberg EP. 2004. Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol 186:1838–1850. doi:10.1128/JB.186.6.1838-1850.2004. PubMed DOI PMC
Knobloch JKM, Horstkotte MA, Rohde H, Kaulfers PM, Mack D. 2002. Alcoholic ingredients in skin disinfectants increase biofilm expression of Staphylococcus epidermidis. J Antimicrob Chemother 49:683–687. doi:10.1093/jac/49.4.683. PubMed DOI
Korem M, Gov Y, Rosenberg M. 2010. Global gene expression in Staphylococcus aureus following exposure to alcohol. Microb Pathog 48:74–84. doi:10.1016/j.micpath.2009.11.002. PubMed DOI
Kastbjerg VG, Larsen MH, Gram L, Ingmer H. 2010. Influence of sublethal concentrations of common disinfectants on expression of virulence genes in Listeria monocytogenes. Appl Environ Microbiol 76:303–309. doi:10.1128/AEM.00925-09. PubMed DOI PMC
Silveira MG, Baumgartner M, Rombouts FM, Abee T. 2004. Effect of adaptation to ethanol on cytoplasmic and membrane protein profiles of Oenococcus oeni. Appl Environ Microbiol 70:2748–2755. doi:10.1128/AEM.70.5.2748-2755.2004. PubMed DOI PMC
Gilbert P, McBain AJ. 2003. Potential impact of increased use of biocides in consumer products on prevalence of antibiotic resistance. Clin Microbiol Rev 16:189–208. doi:10.1128/CMR.16.2.189-208.2003. PubMed DOI PMC
Rolland SL, Carrick TE, Walls AW, McCabe JF. 2007. Dentin decontamination using chloramine T prior to experiments involving bacteria. Dent Mater 23:1468–1472. doi:10.1016/j.dental.2007.01.001. PubMed DOI
Bal Krishna KC, Sathasivan A, Ginige MP. 2013. Microbial community changes with decaying chloramine residuals in a lab-scale system. Water Res 47:4666–4679. doi:10.1016/j.watres.2013.04.035. PubMed DOI
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 116:372–383. doi:10.1016/j.ijfoodmicro.2007.02.017. PubMed DOI
Cincarova L, Polansky O, Babak V, Kulich P, Kralik P. 2016. Changes in the expression of biofilm-associated surface proteins in Staphylococcus aureus food-environmental isolates subjected to sublethal concentrations of disinfectants. Biomed Res Int 2016:4034517. doi:10.1155/2016/4034517. PubMed DOI PMC
Ulrich M, Bastian M, Cramton SE, Ziegler K, Pragman AA, Bragonzi A, Memmi G, Wolz C, Schlievert PM, Cheung A, Döring G. 2007. The staphylococcal respiratory response regulator SrrAB induces ica gene transcription and polysaccharide intercellular adhesin expression, protecting Staphylococcus aureus from neutrophil killing under anaerobic growth conditions. Mol Microbiol 65:1276–1287. doi:10.1111/j.1365-2958.2007.05863.x. PubMed DOI
Archer NK, Mazaitis MJ, Costerton JW, Leid JG, Powers ME, Shirtliff ME. 2011. Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence 2:445–459. doi:10.4161/viru.2.5.17724. PubMed DOI PMC
Houston P, Rowe SE, Pozzi C, Waters EM, O'Gara JP. 2011. Essential role for the major autolysin in the fibronectin-binding protein-mediated Staphylococcus aureus biofilm phenotype. Infect Immun 79:1153–1165. doi:10.1128/IAI.00364-10. PubMed DOI PMC
Nicholas RO, Li T, McDevitt D, Marra A, Sucoloski S, Demarsh PL, Gentry DR. 1999. Isolation and characterization of a sigB deletion mutant of Staphylococcus aureus. Infect Immun 67:3667–3669. PubMed PMC
O'Riordan K, Lee JC. 2004. Staphylococcus aureus capsular polysaccharides. Clin Microbiol Rev 17:218–234. doi:10.1128/CMR.17.1.218-234.2004. PubMed DOI PMC
Cocchiaro JL, Gomez MI, Risley A, Solinga R, Sordelli DO, Lee JC. 2006. Molecular characterization of the capsule locus from non-typeable Staphylococcus aureus. Mol Microbiol 59:948–960. doi:10.1111/j.1365-2958.2005.04978.x. PubMed DOI
Luong TT, Sau K, Roux C, Sau S, Dunman PM, Lee CY. 2011. Staphylococcus aureus ClpC divergently regulates capsule via sae and codY in strain Newman but activates capsule via codY in strain UAMS-1 and in strain Newman with repaired saeS. J Bacteriol 193:686–694. doi:10.1128/JB.00987-10. PubMed DOI PMC
Valle J, Toledo-Arana A, Berasain C, Ghigo JM, Amorena B, Penades JR, Lasa I. 2003. SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus. Mol Microbiol 48:1075–1087. doi:10.1046/j.1365-2958.2003.03493.x. PubMed DOI
Beenken KE, Mrak LN, Griffin LM, Zielinska AK, Shaw LN, Rice KC, Horswill AR, Bayles KW, Smeltzer MS. 2010. Epistatic relationships between sarA and agr in Staphylococcus aureus biofilm formation. PLoS One 5:e10790. doi:10.1371/journal.pone.0010790. PubMed DOI PMC
Chan WC, Coyle BJ, Williams P. 2004. Virulence regulation and quorum sensing in staphylococcal infections: competitive AgrC antagonists as quorum sensing inhibitors. J Med Chem 47:4633–4641. doi:10.1021/jm0400754. PubMed DOI
Boles BR, Horswill AR. 2008. agr-Mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:e1000052. doi:10.1371/journal.ppat.1000052. PubMed DOI PMC
Arya R, Princy SA. 2013. An insight into pleiotropic regulators Agr and Sar: molecular probes paving the new way for antivirulent therapy. Future Microbiol 8:1339–1353. doi:10.2217/fmb.13.92. PubMed DOI
Pratten J, Foster SJ, Chan PF, Wilson M, Nair SP. 2001. Staphylococcus aureus accessory regulators: expression within biofilms and effect on adhesion. Microb Infect 3:633–637. doi:10.1016/S1286-4579(01)01418-6. PubMed DOI
Flannagan RS, Cosio G, Grinstein S. 2009. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7:355–366. doi:10.1038/nrmicro2128. PubMed DOI
Horsburgh MJ, Ingham E, Foster SJ. 2001. In Staphylococcus aureus, Fur is an interactive regulator with PerR, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J Bacteriol 183:468–475. doi:10.1128/JB.183.2.468-475.2001. PubMed DOI PMC
Cosgrove K, Coutts G, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ. 2007. Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol 189:1025–1035. doi:10.1128/JB.01524-06. PubMed DOI PMC
Wolf C, Hochgrafe F, Kusch H, Albrecht D, Hecker M, Engelmann S. 2008. Proteomic analysis of antioxidant strategies of Staphylococcus aureus: diverse responses to different oxidants. Proteomics 8:3139–3153. doi:10.1002/pmic.200701062. PubMed DOI
Ushijima Y, Yoshida O, Villanueva MJ, Ohniwa RL, Morikawa K. 2016. Nucleoid clumping is dispensable for the Dps-dependent hydrogen peroxide resistance in Staphylococcus aureus. Microbiology 162:1822–1828. doi:10.1099/mic.0.000353. PubMed DOI
Michta E, Ding W, Zhu SC, Blin K, Ruan HQ, Wang R, Wohlleben W, Mast Y. 2014. Proteomic approach to reveal the regulatory function of aconitase AcnA in oxidative stress response in the antibiotic producer Streptomyces viridochromogenes Tu494. PLoS One 9:e87905. doi:10.1371/journal.pone.0087905. PubMed DOI PMC
Graham JW, Lei MG, Lee CY. 2013. Trapping and identification of cellular substrates of the Staphylococcus aureus ClpC chaperone. J Bacteriol 195:4506–4516. doi:10.1128/JB.00758-13. PubMed DOI PMC
Chatterjee I, Becker P, Grundmeier M, Bischoff M, Somerville GA, Peters G, Sinha B, Harraghy N, Proctor RA, Herrmann M. 2005. Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J Bacteriol 187:4488–4496. doi:10.1128/JB.187.13.4488-4496.2005. PubMed DOI PMC
Xue T, You Y, Hong D, Sun H, Sun B. 2011. The Staphylococcus aureus KdpDE two-component system couples extracellular K+ sensing and Agr signaling to infection programming. Infect Immun 79:2154–2167. doi:10.1128/IAI.01180-10. PubMed DOI PMC
Resch A, Rosenstein R, Nerz C, Gotz F. 2005. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl Environ Microbiol 71:2663–2676. doi:10.1128/AEM.71.5.2663-2676.2005. PubMed DOI PMC
Makhlin J, Kofman T, Borovok I, Kohler C, Engelmann S, Cohen G, Aharonowitz Y. 2007. Staphylococcus aureus ArcR controls expression of the arginine deiminase operon. J Bacteriol 189:5976–5986. doi:10.1128/JB.00592-07. PubMed DOI PMC
Stepanovic S, Vukovic D, Hola V, Di Bonaventura G, Djukic S, Cirkovic I, Ruzicka F. 2007. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115:891–899. doi:10.1111/j.1600-0463.2007.apm_630.x. PubMed DOI
Ewels P, Magnusson M, Lundin S, Kaller M. 2016. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32:3047–3048. doi:10.1093/bioinformatics/btw354. PubMed DOI PMC
Davis MPA, van Dongen S, Abreu-Goodger C, Bartonicek N, Enright AJ. 2013. Kraken: a set of tools for quality control and analysis of high-throughput sequence data. Methods 63:41–49. doi:10.1016/j.ymeth.2013.06.027. PubMed DOI PMC
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. doi:10.1093/bioinformatics/btu170. PubMed DOI PMC
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21. doi:10.1093/bioinformatics/bts635. PubMed DOI PMC
Wang LG, Wang SQ, Li W. 2012. RSeQC: quality control of RNA-seq experiments. Bioinformatics 28:2184–2185. doi:10.1093/bioinformatics/bts356. PubMed DOI
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:e550. doi:10.1186/s13059-014-0550-8. PubMed DOI PMC
Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. doi:10.1093/bioinformatics/btp616. PubMed DOI PMC
Huber W, Carey VJ, Gentleman R, Anders S, Carlson M, Carvalho BS, Bravo HC, Davis S, Gatto L, Girke T, Gottardo R, Hahne F, Hansen KD, Irizarry RA, Lawrence M, Love MI, MacDonald J, Obenchain V, Oleœ AK, Pagès H, Reyes A, Shannon P, Smyth GK, Tenenbaum D, Waldron L, Morgan M. 2015. Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods 12:115–121. doi:10.1038/nmeth.3252. PubMed DOI PMC
Maere S, Heymans K, Kuiper M. 2005. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448–3449. doi:10.1093/bioinformatics/bti551. PubMed DOI
Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. doi:10.1093/bioinformatics/bti610. PubMed DOI