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Proteomic profile of dormancy within Staphylococcus epidermidis biofilms using iTRAQ and label-free strategies

  • Genomics, transcriptomics, proteomics
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Abstract

Staphylococcus epidermidis is an important nosocomial bacterium among carriers of indwelling medical devices, since it has a strong ability to form biofilms. The presence of dormant bacteria within a biofilm is one of the factors that contribute to biofilm antibiotic tolerance and immune evasion. Here, we provide a detailed characterization of the quantitative proteomic profile of S. epidermidis biofilms with different proportions of dormant bacteria. A total of 427 and 409 proteins were identified by label-free and label-based quantitative methodologies, respectively. From these, 29 proteins were found to be differentially expressed between S. epidermidis biofilms with prevented and induced dormancy. Proteins overexpressed in S. epidermidis with prevented dormancy were associated with ribosome synthesis pathway, which reflects the metabolic state of dormant bacteria. In the opposite, underexpressed proteins were related to catalytic activity and ion binding, with involvement in purine, arginine, and proline metabolism. Additionally, GTPase activity seems to be enhanced in S. epidermidis biofilm with induced dormancy. The role of magnesium in dormancy modulation was further investigated with bioinformatics tool based in predicted interactions. The main molecular function of proteins, which strongly interact with magnesium, was nucleic acid binding. Different proteomic strategies allowed to obtain similar results and evidenced that prevented dormancy led to an expression of a markedly different repertoire of proteins in comparison to the one of dormant biofilms.

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References

  • Abdallah C, Dumas-Gaudot E, Renaut J, Sergeant K (2012) Gel-based and gel-free quantitative proteomics approaches at a glance. Int J Plant Genomics 2012:494–572

    Article  Google Scholar 

  • Alves RM, Vitorino R, Padrao AI, Moreira-Goncalves D, Duarte JA, Ferreira RM, Amado F (2013) iTRAQ-based quantitative proteomic analysis of submandibular glands from rats with STZ-induced hyperglycemia. J Biochem 153:209–220

    Article  CAS  PubMed  Google Scholar 

  • Asakura H, Panutdaporn N, Kawamoto K, Igimi S, Yamamoto S, Makino S (2007) Proteomic characterization of enterohemorrhagic Escherichia coli O157:H7 in the oxidation-induced viable but non-culturable state. Microbiol Immunol 51:875–881

    Article  CAS  PubMed  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Balaban NQ, Gerdes K, Lewis K, McKinney JD (2013) A problem of persistence: still more questions than answers? Nat Rev Microbiol 11:587–591

    Article  CAS  PubMed  Google Scholar 

  • Berghoff BA, Konzer A, Mank NN, Looso M, Rische T, Forstner KU, Kruger M, Klug G (2013) Integrative “omics”-approach discovers dynamic and regulatory features of bacterial stress responses. PLoS Genet 9, e1003576

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bhatt AN, Shukla N, Aliverti A, Zanetti G, Bhakuni V (2005) Modulation of cooperativity in Mycobacterium tuberculosis NADPH-ferredoxin reductase: cation-and pH-induced alterations in native conformation and destabilization of the NADP+-binding domain. Protein Sci 14:980–992

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cain JA, Solis N, Cordwell SJ (2013) Beyond gene expression: the impact of protein post-translational modifications in bacteria. J Proteomics 97:265–286

    Article  PubMed  Google Scholar 

  • Carvalhais V, Franca A, Cerca F, Vitorino R, Pier GB, Vilanova M, Cerca N (2014) Dormancy within Staphylococcus epidermidis biofilms: a transcriptomic analysis by RNA-seq. Appl Microbiol Biotechnol 98:2585–2596

    Article  CAS  PubMed  Google Scholar 

  • Carvalhais V, Franca A, Pier GB, Vilanova M, Cerca N, Vitorino R (2015) Comparative proteomic and transcriptomic profile of Staphylococcus epidermidis biofilms grown in glucose-enriched medium. Talanta 132:705–712

    Article  CAS  PubMed  Google Scholar 

  • Cashel M, Gentry D, Hernandez V, Vinella D (1996) The stringent response. In: Neidhardt FC, Curtiss IIIR, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed) Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. AMS Press, Washington DC, pp 1458–1496

  • Cerca N, Martins S, Cerca F, Jefferson KK, Pier GB, Oliveira R, Azeredo J (2005) Comparative assessment of antibiotic susceptibility of coagulase-negative staphylococci in biofilm versus planktonic culture as assessed by bacterial enumeration or rapid XTT colorimetry. J Antimicrob Chemother 56:331–336

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cerca N, Jefferson KK, Oliveira R, Pier GB, Azeredo J (2006) Comparative antibody-mediated phagocytosis of Staphylococcus epidermidis cells grown in a biofilm or in the planktonic state. Infect Immun 74:4849–4855

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cerca F, Andrade F, Franca A, Andrade EB, Ribeiro A, Almeida AA, Cerca N, Pier G, Azeredo J, Vilanova M (2011) Staphylococcus epidermidis biofilms with higher proportions of dormant bacteria induce a lower activation of murine macrophages. J Med Microbiol 60:1717–1724

    Article  PubMed  Google Scholar 

  • Cerca F, Franca A, Perez-Cabezas B, Carvalhais V, Ribeiro A, Azeredo J, Pier GB, Cerca N, Vilanova M (2014) Dormant bacteria within Staphylococcus epidermidis biofilms have low inflammatory properties and maintain tolerance to vancomycin and penicillin after entering planktonic growth. J Med Microbiol 63:1274–1283

    Article  CAS  PubMed  Google Scholar 

  • Conrad CC, Choi J, Malakowsky CA, Talent JM, Dai R, Marshall P, Gracy RW (2001) Identification of protein carbonyls after two-dimensional electrophoresis. Proteomics 1:829–834

    Article  CAS  PubMed  Google Scholar 

  • Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penades JR (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183:2888–2896

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cutinelli C, Galdiero F (1967) Ion-binding properties of the cell wall of Staphylococcus aureus. J Bacteriol 93:2022–2023

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dalle-Donne I, Carini M, Orioli M, Vistoli G, Regazzoni L, Colombo G, Rossi R, Milzani A, Aldini G (2009) Protein carbonylation: 2,4-dinitrophenylhydrazine reacts with both aldehydes/ketones and sulfenic acids. Free Radic Biol Med 46:1411–1419

    Article  CAS  PubMed  Google Scholar 

  • de Sousa AR, Penalva LO, Marcotte EM, Vogel C (2009) Global signatures of protein and mRNA expression levels. Mol BioSyst 5:1512–1526

    Google Scholar 

  • Dean RT, Fu S, Stocker R, Davies MJ (1997) Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 324:1–18

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Deng X, Weerapana E, Ulanovskaya O, Sun F, Liang H, Ji Q, Ye Y, Fu Y, Zhou L, Li J, Zhang H, Wang C, Alvarez S, Hicks LM, Lan L, Wu M, Cravatt BF, He C (2013) Proteome-wide quantification and characterization of oxidation-sensitive cysteines in pathogenic bacteria. Cell Host Microbe 13:358–370

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Donlan RM (2001) Biofilms and device-associated infections. Emerg Infect Dis 7:277–281

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dorr T, Vulic M, Lewis K (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8, e1000317

    Article  PubMed Central  PubMed  Google Scholar 

  • Doyle RJ, Matthews TH, Streips UN (1980) Chemical basis for selectivity of metal ions by the Bacillus subtilis cell wall. J Bacteriol 143:471–480

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dunne v Jr, Burd EM (1992) The effects of magnesium, calcium, EDTA, and pH on the in vitro adhesion of Staphylococcus epidermidis to plastic. Microbiol Immunol 36:1019–1027

    Article  CAS  PubMed  Google Scholar 

  • Fey PD (2010) Modality of bacterial growth presents unique targets: how do we treat biofilm-mediated infections? Curr Opin Microbiol 13:610–615

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fey PD, Olson ME (2010) Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiol 5:917–933

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fozo EM, Makarova KS, Shabalina SA, Yutin N, Koonin EV, Storz G (2010) Abundance of type I toxin-antitoxin systems in bacteria: searches for new candidates and discovery of novel families. Nucleic Acids Res 38:3743–3759

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von Mering C, Jensen LJ (2013) STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41:D808–D815

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gaupp R, Ledala N, Somerville GA (2012) Staphylococcal response to oxidative stress. Front Cell Infect Microbiol 2:33

    Article  PubMed Central  PubMed  Google Scholar 

  • Goeders N, Van Melderen L (2014) Toxin-antitoxin systems as multilevel interaction systems. Toxins (Basel) 6:304–324

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Groisman EA, Hollands K, Kriner MA, Lee EJ, Park SY, Pontes MH (2013) Bacterial Mg2+ homeostasis, transport, and virulence. Annu Rev Genet 47:625–646

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guell M, Yus E, Lluch-Senar M, Serrano L (2011) Bacterial transcriptomics: what is beyond the RNA horiz-ome? Nat Rev Microbiol 9:658–669

    Article  PubMed  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    Article  CAS  PubMed  Google Scholar 

  • Heilmann C, Hussain M, Peters G, Gotz F (1997) Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 5:1013–1024

    Article  Google Scholar 

  • Heim S, Lleo M, Bonato B, Guzman CA, Canepari P (2002) The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. J Bacteriol 184:6739–6745

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hong SH, Wang X, O’Connor HF, Benedik MJ, Wood TK (2012) Bacterial persistence increases as environmental fitness decreases. Microb Biotechnol 5:509–522

    Article  PubMed Central  PubMed  Google Scholar 

  • Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4:1265–1272

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277–D280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaprelyants AS, Gottschal JC, Kell DB (1993) Dormancy in non-sporulating bacteria. FEMS Microbiol Rev 10:271–285

    Article  CAS  PubMed  Google Scholar 

  • Keren I, Shah D, Spoering A, Kaldalu N, Lewis K (2004) Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 186:8172–8180

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kuhn M, Szklarczyk D, Pletscher-Frankild S, Blicher TH, von Mering C, Jensen LJ, Bork P (2014) STITCH 4: integration of protein-chemical interactions with user data. Nucleic Acids Res 42:D401–D407

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lasa I, Penades JR (2006) Bap: a family of surface proteins involved in biofilm formation. Res Microbiol 157:99–107

    Article  CAS  PubMed  Google Scholar 

  • Lellouche J, Friedman A, Lahmi R, Gedanken A, Banin E (2012) Antibiofilm surface functionalization of catheters by magnesium fluoride nanoparticles. Int J Nanomedicine 7:1175–1188

    PubMed Central  CAS  PubMed  Google Scholar 

  • Leszczynska D, Matuszewska E, Kuczynska-Wisnik D, Furmanek-Blaszk B, Laskowska E (2013) The formation of persister cells in stationary-phase cultures of Escherichia coli is associated with the aggregation of endogenous proteins. PLoS One 8, e54737

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lewis K (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5:48–56

    Article  CAS  PubMed  Google Scholar 

  • Liebler DC (2008) Protein damage by reactive electrophiles: targets and consequences. Chem Res Toxicol 21:117–128

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mack D, Siemssen N, Laufs R (1992) Parallel induction by glucose of ahderence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion. Infect Immun 60:2048–2057

    PubMed Central  CAS  PubMed  Google Scholar 

  • Maisonneuve E, Castro-Camargo M, Gerdes K (2013) (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154:1140–1150

    Article  CAS  PubMed  Google Scholar 

  • Oliveros JC (2007) VENNY. An interactive tool for comparing lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/

  • Orman MA, Brynildsen MP (2013) Dormancy is not necessary or sufficient for bacterial persistence. Antimicrob Agents Chemother 57:3230–3239

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Otto M (2012) Molecular basis of Staphylococcus epidermidis infections. Semin Immunopathol 34:201–214

    Article  PubMed Central  PubMed  Google Scholar 

  • Otto M (2013) Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu Rev Med 64:175–188

    Article  CAS  PubMed  Google Scholar 

  • Otto M (2014) Staphylococcus epidermidis pathogenesis. Methods Mol Biol 1106:17–31

    Article  CAS  PubMed  Google Scholar 

  • Park PW, Rosenbloom J, Abrams WR, Rosenbloom J, Mecham RP (1996) Molecular cloning and expression of the gene for elastin-binding protein (ebpS) in Staphylococcus aureus. J Biol Chem 271:15803–15809

    Article  CAS  PubMed  Google Scholar 

  • Piddington DL, Kashkouli A, Buchmeier NA (2000) Growth of Mycobacterium tuberculosis in a defined medium is very restricted by acid pH and Mg2+ levels. Infect Immun 68:4518–4522

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pinto D, Santos MA, Chambel L (2013) Thirty years of viable but nonculturable state research: Unsolved molecular mechanisms. Crit Rev Microbiol 41:61–76

  • Potrykus K, Cashel M (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62:35–51

    Article  CAS  PubMed  Google Scholar 

  • Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, Molin S, Qu D (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153:2083–2092

    Article  CAS  PubMed  Google Scholar 

  • Robinson CE, Keshavarzian A, Pasco DS, Frommel TO, Winship DH, Holmes EW (1999) Determination of protein carbonyl groups by immunoblotting. Anal Biochem 266:48–57

    Article  CAS  PubMed  Google Scholar 

  • Rohde H, Burdelski C, Bartscht K, Hussain M, Buck F, Horstkotte MA, Knobloch JK, Heilmann C, Herrmann M, Mack D (2005) Induction of Staphylococcus epidermidis biofilm formation via proteolytic processing of the accumulation-associated protein by staphylococcal and host proteases. Mol Microbiol 55:1883–1895

    Article  CAS  PubMed  Google Scholar 

  • Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3:1154–1169

    Article  CAS  PubMed  Google Scholar 

  • Sadovskaya I, Vinogradov E, Li J, Jabbouri S (2004) Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus epidermidis RP62A, a reference biofilm-positive strain. Carbohydr Res 339:1467–1473

    Article  CAS  PubMed  Google Scholar 

  • Sadovskaya I, Vinogradov E, Flahaut S, Kogan G, Jabbouri S (2005) Extracellular carbohydrate-containing polymers of a model biofilm-producing strain, Staphylococcus epidermidis RP62A. Infect Immun 73:3007–3017

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sanchez R, Riddle M, Woo J, Momand J (2008) Prediction of reversibly oxidized protein cysteine thiols using protein structure properties. Protein Sci 17:473–481

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sayed N, Nonin-Lecomte S, Rety S, Felden B (2012) Functional and structural insights of a Staphylococcus aureus apoptotic-like membrane peptide from a toxin-antitoxin module. J Biol Chem 287:43454–43463

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sonenshein AL (2005) CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr Opin Microbiol 8:203–207

    Article  CAS  PubMed  Google Scholar 

  • Song B, Leff LG (2006) Influence of magnesium ions on biofilm formation by Pseudomonas fluorescens. Microbiol Res 161:355–361

    Article  CAS  PubMed  Google Scholar 

  • Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210

    Article  CAS  PubMed  Google Scholar 

  • Straub L (2011) Beyond the transcripts: what controls protein variation? PLoS Biol 9, e1001146

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thompson A, Schafer J, Kuhn K, Kienle S, Schwarz J, Schmidt G, Neumann T, Johnstone R, Mohammed AK, Hamon C (2003) Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 75:1895–1904

    Article  CAS  PubMed  Google Scholar 

  • Unterholzner SJ, Poppenberger B, Rozhon W (2013) Toxin-antitoxin systems: Biology, identification, and application. Mob Genet Elements 3, e26219

    Article  PubMed Central  PubMed  Google Scholar 

  • Verstraeten N, Fauvart M, Versees W, Michiels J (2011) The universally conserved prokaryotic GTPases. Microbiol Mol Biol Rev 75:507–542

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vitorino R, Guedes S, Manadas B, Ferreira R, Amado F (2012) Toward a standardized saliva proteome analysis methodology. J Proteomics 75:5140–5165

    Article  CAS  PubMed  Google Scholar 

  • Vuong C, Kocianova S, Voyich JM, Yao Y, Fischer ER, DeLeo FR, Otto M (2004) A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279:54881–54886

    Article  CAS  PubMed  Google Scholar 

  • Wakamoto Y, Dhar N, Chait R, Schneider K, Signorino-Gelo F, Leibler S, McKinney JD (2013) Dynamic persistence of antibiotic-stressed mycobacteria. Science 339:91–95

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Khan BA, Cheung GY, Bach TH, Jameson-Lee M, Kong KF, Queck SY, Otto M (2011) Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice. J Clin Invest 121:238–248

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Williamson KS, Richards LA, Perez-Osorio AC, Pitts B, McInnerney K, Stewart PS, Franklin MJ (2012) Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population. J Bacteriol 194:2062–2073

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang W, Li F, Nie L (2010) Integrating multiple ‘omics’ analysis for microbial biology: application and methodologies. Microbiology 156:287–301

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was funded by Fundação para a Ciência e a Tecnologia (FCT) and COMPETE grants PTDC/BIA-MIC/113450/2009, FCOMP-01-0124-FEDER-014309, QOPNA research unit (project PEst-C/QUI/UI0062/2013), RNEM (National Mass Spectrometry Network), and CENTRO-07-ST24-FEDER-002034. The authors also thank the FCT Strategic Project PEst-OE/EQB/LA0023/2013, the Project NORTE-07-0124-FEDER-000027, co-funded by the Programa Operacional Regional do Norte (ON.2 – O Novo Norte), QREN, FEDER, and the project RECI/EBB-EBI/0179/2012, FCOMP-01-0124-FEDER-027462. VC has an individual FCT fellowship (SFRH/BD/78235/2011). NC is an Investigator FCT.

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Authors and Affiliations

  1. Centre of Biological Engineering (CEB), Laboratory of Research in Biofilms Rosário Oliveira (LIBRO), University of Minho, Campus de Gualtar, 4710-057, Braga, Portugal

    Virginia Carvalhais & Nuno Cerca

  2. QOPNA, Mass Spectrometry Center, Department of Chemistry, University of Aveiro, 3810-193, Aveiro, Portugal

    Virginia Carvalhais & Rui Vitorino

  3. Instituto de Biologia Molecular e Celular (IBMC), Rua do Campo Alegre 83, Porto, Portugal

    Manuel Vilanova

  4. Instituto de Ciências Biomédicas Abel Salazar (ICBAS), University of Porto, Rua de Rua de Jorge Viterbo Ferreira 228, 4050-313, Porto, Portugal

    Manuel Vilanova

  5. University of Aveiro, Aveiro, Portugal

    Rui Vitorino

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  1. Virginia Carvalhais
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  4. Rui Vitorino
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Correspondence to Rui Vitorino.

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Carvalhais, V., Cerca, N., Vilanova, M. et al. Proteomic profile of dormancy within Staphylococcus epidermidis biofilms using iTRAQ and label-free strategies. Appl Microbiol Biotechnol 99, 2751–2762 (2015). https://doi.org/10.1007/s00253-015-6434-3

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