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ICREA","award":["628"],"award-info":[{"award-number":["628"]}]},{"name":"SGR-Generalitat de Catalunya and ICREA","award":["FI19\/00090"],"award-info":[{"award-number":["FI19\/00090"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Objectives: To evaluate the expression dynamics of biofilm genes in methicillin-resistant Staphylococcus aureus (MRSA) retrieved from endotracheal tubes (ETT) and to determine how gene regulation is attenuated in vitro where host\u2013environmental factors are no longer present. Methods: Biofilm was grown (24 h) in tryptic broth soy plus 0.25% glucose for a clinical MRSA isolate in planktonic state and after sessile growth named ETT-MRSA (S2, S3, S4, S5, S6, S7). Gene expression of five biofilm-related genes (icaC, clfB, ebps, fnbB, and RNA\u00a0III) was assessed consecutively from day 1 to day 4 after ETT growth through real-time PCR. 16S rRNA was used as a control. Results: The MRSA isolates retrieved from ETT were capable of producing biofilms dependent on ica. The gene expression dynamics of ETT-MRSA changed progressively compared to planktonic MRSA gene expression under both ambient air (p &lt; 0.001) and ambient air with 5% CO2 (p &lt; 0.001). Dynamic assessment of icaC expression in both atmospheric conditions showed progressive downregulation in vitro compared to in vivo ETT biofilms. The expression patterns of clfB and ebps genes were similar to icaC. In contrast, the expression of the RNA III gene showed progressive upregulation from day 1 to day 4 (p &lt; 0.001). Conclusions: MRSA loses its biofilm gene expression in vitro, by adaptive features across multiple generations, as evidenced by the progressive downregulation of icaC and upregulation of RNA III. These findings underscore the significance of host\u2013environment dependence in regulating bacterial biofilm genes, highlighting its importance in diagnostics. Bacterial strains lose their host-specific characteristics as they are cultured in vitro.<\/jats:p>","DOI":"10.3390\/pathogens13020144","type":"journal-article","created":{"date-parts":[[2024,2,6]],"date-time":"2024-02-06T03:22:31Z","timestamp":1707189751000},"page":"144","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Bacterial Adaptive Memory in Methicillin-Resistant Staphylococcus aureus from Endotracheal Tubes"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7528-9636","authenticated-orcid":false,"given":"Laia","family":"Fern\u00e1ndez-Barat","sequence":"first","affiliation":[{"name":"Centro de Investigaci\u00f3n Biomedica En Red-Enfermedades Respiratorias (CibeRes, CB06\/06\/0028) and Institut d\u2019Investigacions Biom\u00e8diques August Pi i Sunyer (IDIBAPS), 08036 Barcelona, Spain"},{"name":"University of Barcelona, 08193 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ruben","family":"L\u00f3pez-Aladid","sequence":"additional","affiliation":[{"name":"Centro de Investigaci\u00f3n Biomedica En Red-Enfermedades Respiratorias (CibeRes, CB06\/06\/0028) and Institut d\u2019Investigacions Biom\u00e8diques August Pi i Sunyer (IDIBAPS), 08036 Barcelona, Spain"},{"name":"University of Barcelona, 08193 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nil","family":"V\u00e1zquez","sequence":"additional","affiliation":[{"name":"Centro de Investigaci\u00f3n Biomedica En Red-Enfermedades Respiratorias (CibeRes, CB06\/06\/0028) and Institut d\u2019Investigacions Biom\u00e8diques August Pi i Sunyer (IDIBAPS), 08036 Barcelona, Spain"},{"name":"University of Barcelona, 08193 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roberto","family":"Cabrera","sequence":"additional","affiliation":[{"name":"Centro de Investigaci\u00f3n Biomedica En Red-Enfermedades Respiratorias (CibeRes, CB06\/06\/0028) and Institut d\u2019Investigacions Biom\u00e8diques August Pi i Sunyer (IDIBAPS), 08036 Barcelona, Spain"},{"name":"University of Barcelona, 08193 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8025-3926","authenticated-orcid":false,"given":"Jordi","family":"Vila","sequence":"additional","affiliation":[{"name":"University of Barcelona, 08193 Barcelona, Spain"},{"name":"Microbiology Service at Hospital Clinic and Institute of Global Health (ISGlobal), 08036 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Miquel","family":"Ferrer","sequence":"additional","affiliation":[{"name":"Centro de Investigaci\u00f3n Biomedica En Red-Enfermedades Respiratorias (CibeRes, CB06\/06\/0028) and Institut d\u2019Investigacions Biom\u00e8diques August Pi i Sunyer (IDIBAPS), 08036 Barcelona, Spain"},{"name":"University of Barcelona, 08193 Barcelona, Spain"},{"name":"Pulmonary and Critical Care Unit, Respiratory Institute, Hospital Clinic, 08036 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8643-2167","authenticated-orcid":false,"given":"Antoni","family":"Torres","sequence":"additional","affiliation":[{"name":"Centro de Investigaci\u00f3n Biomedica En Red-Enfermedades Respiratorias (CibeRes, CB06\/06\/0028) and Institut d\u2019Investigacions Biom\u00e8diques August Pi i Sunyer (IDIBAPS), 08036 Barcelona, Spain"},{"name":"University of Barcelona, 08193 Barcelona, Spain"},{"name":"Pulmonary and Critical Care Unit, Respiratory Institute, Hospital Clinic, 08036 Barcelona, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,2,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1599","DOI":"10.2217\/fmb-2016-0040","article-title":"Biofilms in Ventilator-Associated Pneumonia","volume":"11","author":"Torres","year":"2016","journal-title":"Future Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1700582","DOI":"10.1183\/13993003.00582-2017","article-title":"International ERS\/ESICM\/ESCMID\/ALAT Guidelines for the Management of Hospital-Acquired Pneumonia and Ventilator-Associated Pneumonia: Guidelines for the Management of Hospital-Acquired Pneumonia (HAP)\/Ventilator-Associated Pneumonia (VAP) of the European Respiratory Society (ERS), European Society of Intensive Care Medicine (ESICM), European Society of Clinical Microbiology and Infectious Diseases (ESCMID) and Asociaci\u00f3n Latinoamericana Del T\u00f3rax (ALAT)","volume":"50","author":"Torres","year":"2017","journal-title":"Eur. Respir. J."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"S1","DOI":"10.1016\/j.cmi.2014.10.024","article-title":"ESCMID Guideline for the Diagnosis and Treatment of Biofilm Infections 2014","volume":"21","author":"Bjarnsholt","year":"2015","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_4","unstructured":"European Centre for Disease Prevention and Control (2023). Annual Epidemiological Report for 2019\u2013Healthcareassociated Infections Acquired in Intensive Care Units, ECDC. Annual Epidemiological Report for 2018."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"996","DOI":"10.1128\/jcm.22.6.996-1006.1985","article-title":"Adherence of Coagulase-Negative Staphylococci to Plastic Tissue Culture Plates: A Quantitative Model for the Adherence of Staphylococci to Medical Devices","volume":"22","author":"Christensen","year":"1985","journal-title":"J. Clin. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"725","DOI":"10.2217\/fmb.14.33","article-title":"Evaluation of Different Microtiter Plate-Based Methods for the Quantitative Assessment of Staphylococcus Aureus Biofilms","volume":"9","author":"Elkhatib","year":"2014","journal-title":"Future Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"288","DOI":"10.3390\/pathogens2020288","article-title":"From in Vitro to in Vivo Models of Bacterial Biofilm-Related Infections","volume":"2","author":"Lebeaux","year":"2013","journal-title":"Pathogens"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Manandhar, S., Singh, A., Varma, A., Pandey, S., and Shrivastava, N. (2018). Evaluation of Methods to Detect in Vitro Biofilm Formation by Staphylococcal Clinical Isolates. BMC Res. Notes, 11.","DOI":"10.1186\/s13104-018-3820-9"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"ftw057","DOI":"10.1093\/femspd\/ftw057","article-title":"Preliminary Results of a New Antibiotic Susceptibility Test against Biofilm Installation in Device-Associated Infections: The Antibiofilmogram\u00ae","volume":"74","author":"Tasse","year":"2016","journal-title":"Pathog. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Pozzi, C., Waters, E.M., Rudkin, J.K., Schaeffer, C.R., Lohan, A.J., Tong, P., Loftus, B.J., Pier, G.B., Fey, P.D., and Massey, R.C. (2012). Methicillin Resistance Alters the Biofilm Phenotype and Attenuates Virulence in Staphylococcus Aureus Device-Associated Infections. PLoS Pathog., 8.","DOI":"10.1371\/journal.ppat.1002626"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.meegid.2013.05.002","article-title":"Quantitative PCR Analysis of Genes Expressed during Biofilm Development of Methicillin Resistant Staphylococcus Aureus (MRSA)","volume":"18","author":"Atshan","year":"2013","journal-title":"Infect. Genet. Evol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1016\/j.rvsc.2008.01.005","article-title":"Biofilm-Forming Associated Genotypic and Phenotypic Characteristics of Staphylococcus Spp. Isolated from Animals and Air","volume":"85","author":"Seo","year":"2008","journal-title":"Res. Vet. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"14036","DOI":"10.1073\/pnas.1509251112","article-title":"RNAIII of the Staphylococcus Aureus Agr System Activates Global Regulator MgrA by Stabilizing mRNA","volume":"112","author":"Gupta","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"11906","DOI":"10.1038\/s41598-018-30494-7","article-title":"Assessment of in Vivo versus in Vitro Biofilm Formation of Clinical Methicillin-Resistant Staphylococcus Aureus Isolates from Endotracheal Tubes","volume":"8","author":"Motos","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2018","DOI":"10.1038\/s41396-019-0412-1","article-title":"Establishment of an Induced Memory Response in Pseudomonas Aeruginosa during Infection of a Eukaryotic Host","volume":"13","author":"Kordes","year":"2019","journal-title":"ISME J."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1186\/s13054-019-2523-5","article-title":"Comparative Efficacy of Linezolid and Vancomycin for Endotracheal Tube MRSA Biofilms from ICU Patients","volume":"23","author":"Motos","year":"2019","journal-title":"Crit. Care"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Di Domenico, E.G., Toma, L., Provot, C., Ascenzioni, F., Sperduti, I., Prignano, G., Gallo, M.T., Pimpinelli, F., Bordignon, V., and Bernardi, T. (2016). Development of an in Vitro Assay, Based on the BioFilm Ring Test\u00ae, for Rapid Profiling of Biofilm-Growing Bacteria. Front. Microbiol., 7.","DOI":"10.3389\/fmicb.2016.01429"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Fran\u00e7a, A., Melo, L.D., and Cerca, N. (2011). Comparison of RNA Extraction Methods from Biofilm Samples of Staphylococcus Epidermidis. BMC Res. Notes, 4.","DOI":"10.1186\/1756-0500-4-572"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1038\/nature12804","article-title":"Memory and Modularity in Cell-Fate Decision Making","volume":"503","author":"Norman","year":"2013","journal-title":"Nature"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Lambert, G., and Kussell, E. (2014). Memory and Fitness Optimization of Bacteria under Fluctuating Environments. PLoS Genet., 10.","DOI":"10.1371\/journal.pgen.1004556"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"4471","DOI":"10.1073\/pnas.1720071115","article-title":"Multigenerational Memory and Adaptive Adhesion in Early Bacterial Biofilm Communities","volume":"115","author":"Lee","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e01008-18","DOI":"10.1128\/AEM.01008-18","article-title":"MgrA Negatively Regulates Biofilm Formation and Detachment by Repressing the Expression of Psm Operons in Staphylococcus Aureus","volume":"84","author":"Jiang","year":"2018","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.molcel.2008.08.005","article-title":"RNAIII-Independent Target Gene Control by the Agr Quorum-Sensing System: Insight into the Evolution of Virulence Regulation in Staphylococcus Aureus","volume":"32","author":"Queck","year":"2008","journal-title":"Mol. Cell"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Kim, M.K., Zhao, A., Wang, A., Brown, Z.Z., Muir, T.W., Stone, H.A., and Bassler, B.L. (2017). Surface-Attached Molecules Control Staphylococcus Aureus Quorum Sensing and Biofilm Development. Nat. Microbiol., 2.","DOI":"10.1038\/nmicrobiol.2017.80"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1007\/s00284-008-9211-z","article-title":"Effect of Different Incubation Atmospheres on the Production of Biofilm in Methicillin-Resistant Staphylococcus Aureus (MRSA) Grown in Nutrient-Limited Medium","volume":"57","author":"Ursic","year":"2008","journal-title":"Curr. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2878","DOI":"10.1128\/JCM.00520-10","article-title":"Clinical and Molecular Characteristics of Infections with CO2-Dependent Small-Colony Variants of Staphylococcus Aureus","volume":"48","author":"Acosta","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.jiac.2014.10.001","article-title":"Effect of Incubation Atmosphere on the Production and Composition of Staphylococcal Biofilms","volume":"21","author":"Asai","year":"2015","journal-title":"J. Infect. Chemother."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4079","DOI":"10.1128\/IAI.69.6.4079-4085.2001","article-title":"Anaerobic Conditions Induce Expression of Polysaccharide Intercellular Adhesin in Staphylococcus Aureus and Staphylococcus Epidermidis","volume":"69","author":"Cramton","year":"2001","journal-title":"Infect. Immun."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/13\/2\/144\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T13:55:23Z","timestamp":1760104523000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/13\/2\/144"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,2,5]]},"references-count":28,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2024,2]]}},"alternative-id":["pathogens13020144"],"URL":"https:\/\/doi.org\/10.3390\/pathogens13020144","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,2,5]]}}}