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

Applied Microbiology and Biotechnology

Volumn 99, Issue 6, 2015, Pages 2751-2762

  Carvalhais, Virginia ^a,b   Cerca, Nuno ^a   Vilanova, Manuel ^c,d   Vitorino, Rui ^b  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF AVEIRO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

Author keywords

Carbonylation; Dormancy; emPAI; iTRAQ; Quantitative proteomics; Staphylococcus epidermidis biofilm

Indexed keywords

AMINO ACIDS; BACTERIA; BIOFILMS; BIOINFORMATICS; BIOMEDICAL EQUIPMENT; BIOSYNTHESIS; CARBONYLATION; CATALYST ACTIVITY; MAGNESIUM; METABOLISM; MOLECULAR BIOLOGY; NUCLEIC ACIDS;

DORMANCY; EMPAI; ITRAQ; QUANTITATIVE PROTEOMICS; STAPHYLOCOCCUS EPIDERMIDIS BIOFILMS;

PROTEINS;

ARGININE; BACTERIAL PROTEIN; GUANOSINE TRIPHOSPHATASE; MAGNESIUM; PROLINE; PROTEOME; PURINE;

AMINO ACID METABOLISM; ARTICLE; BACTERIAL METABOLISM; BIOFILM; DORMANCY; ENZYME ACTIVITY; FUNCTIONAL PROTEOMICS; ISOBARIC TAGS FOR RELATIVE AND ABSOLUTE QUANTITATION; ISOTOPE LABELING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN CARBONYLATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; STAPHYLOCOCCUS EPIDERMIDIS; BIOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; TANDEM MASS SPECTROMETRY;

BACTERIAL PROTEINS; BIOFILMS; COMPUTATIONAL BIOLOGY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MAGNESIUM; PROTEOME; STAPHYLOCOCCUS EPIDERMIDIS; TANDEM MASS SPECTROMETRY;

EID: 84925485159     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6434-3     Document Type: Article

References (80)

1. 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
2. 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
3. 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
4. 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
5. Balaban NQ, Gerdes K, Lewis K, McKinney JD (2013) A problem of persistence: still more questions than answers? Nat Rev Microbiol 11:587–591
6. 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
7. +-binding domain. Protein Sci 14:980–992
8. Cain JA, Solis N, Cordwell SJ (2013) Beyond gene expression: the impact of protein post-translational modifications in bacteria. J Proteomics 97:265–286
9. 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
10. 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
11. 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
12. 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
13. 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
14. 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
15. 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
16. 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
17. 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
18. Cutinelli C, Galdiero F (1967) Ion-binding properties of the cell wall of Staphylococcus aureus. J Bacteriol 93:2022–2023
19. 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
20. de Sousa AR, Penalva LO, Marcotte EM, Vogel C (2009) Global signatures of protein and mRNA expression levels. Mol BioSyst 5:1512–1526
21. Dean RT, Fu S, Stocker R, Davies MJ (1997) Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 324:1–18
22. 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
23. Donlan RM (2001) Biofilms and device-associated infections. Emerg Infect Dis 7:277–281
24. Dorr T, Vulic M, Lewis K (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8, e1000317
25. 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
26. 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
27. Fey PD (2010) Modality of bacterial growth presents unique targets: how do we treat biofilm-mediated infections? Curr Opin Microbiol 13:610–615
28. Fey PD, Olson ME (2010) Current concepts in biofilm formation of Staphylococcus epidermidis. Future Microbiol 5:917–933
29. 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
30. 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
31. Gaupp R, Ledala N, Somerville GA (2012) Staphylococcal response to oxidative stress. Front Cell Infect Microbiol 2:33
32. Goeders N, Van Melderen L (2014) Toxin-antitoxin systems as multilevel interaction systems. Toxins (Basel) 6:304–324
33. 2+ homeostasis, transport, and virulence. Annu Rev Genet 47:625–646
34. 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
35. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108
36. 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
37. 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
38. Hong SH, Wang X, O’Connor HF, Benedik MJ, Wood TK (2012) Bacterial persistence increases as environmental fitness decreases. Microb Biotechnol 5:509–522
39. 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
40. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277–D280
41. Kaprelyants AS, Gottschal JC, Kell DB (1993) Dormancy in non-sporulating bacteria. FEMS Microbiol Rev 10:271–285
42. 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
43. 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
44. Lasa I, Penades JR (2006) Bap: a family of surface proteins involved in biofilm formation. Res Microbiol 157:99–107
45. 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
46. 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
47. Lewis K (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5:48–56
48. Liebler DC (2008) Protein damage by reactive electrophiles: targets and consequences. Chem Res Toxicol 21:117–128
49. 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
50. Maisonneuve E, Castro-Camargo M, Gerdes K (2013) (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154:1140–1150
51. Oliveros JC (2007) VENNY. An interactive tool for comparing lists with Venn Diagrams. http://bioinfogp.cnb.csic.es/tools/venny/
52. Orman MA, Brynildsen MP (2013) Dormancy is not necessary or sufficient for bacterial persistence. Antimicrob Agents Chemother 57:3230–3239
53. Otto M (2012) Molecular basis of Staphylococcus epidermidis infections. Semin Immunopathol 34:201–214
54. Otto M (2013) Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity. Annu Rev Med 64:175–188
55. Otto M (2014) Staphylococcus epidermidis pathogenesis. Methods Mol Biol 1106:17–31
56. 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
57. 2+ levels. Infect Immun 68:4518–4522
58. Pinto D, Santos MA, Chambel L (2013) Thirty years of viable but nonculturable state research: Unsolved molecular mechanisms. Crit Rev Microbiol 41:61–76
59. Potrykus K, Cashel M (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62:35–51
60. 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
61. 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
62. 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
63. 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
64. 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
65. 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
66. 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
67. 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
68. Sonenshein AL (2005) CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr Opin Microbiol 8:203–207
69. Song B, Leff LG (2006) Influence of magnesium ions on biofilm formation by Pseudomonas fluorescens. Microbiol Res 161:355–361
70. Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210
71. Straub L (2011) Beyond the transcripts: what controls protein variation? PLoS Biol 9, e1001146
72. 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
73. Unterholzner SJ, Poppenberger B, Rozhon W (2013) Toxin-antitoxin systems: Biology, identification, and application. Mob Genet Elements 3, e26219
74. Verstraeten N, Fauvart M, Versees W, Michiels J (2011) The universally conserved prokaryotic GTPases. Microbiol Mol Biol Rev 75:507–542
75. Vitorino R, Guedes S, Manadas B, Ferreira R, Amado F (2012) Toward a standardized saliva proteome analysis methodology. J Proteomics 75:5140–5165
76. 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
77. 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
78. 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
79. 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
80. Zhang W, Li F, Nie L (2010) Integrating multiple ‘omics’ analysis for microbial biology: application and methodologies. Microbiology 156:287–301