Role of environmental and antibiotic stress on Staphylococcus epidermidis biofilm microstructure

Langmuir

Volumn 29, Issue 23, 2013, Pages 7017-7024

  Stewart, Elizabeth J ^a   Satorius, Ashley E ^b   Younger, John G ^b   Solomon, Michael J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFOCAL LASER SCANNING MICROSCOPY; FRACTURE AND FRAGMENTATIONS; IMAGE ANALYSIS TECHNIQUES; RADIAL DISTRIBUTION FUNCTIONS; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS EPIDERMIDIS BIOFILMS; STRUCTURE CHARACTERISTIC; TRANSPORT AND MECHANICAL PROPERTIES;

ANTIBIOTICS; BIOMECHANICS; CELL PROLIFERATION; GROWTH KINETICS; MECHANICAL PROPERTIES;

BIOFILMS;

ANTIINFECTIVE AGENT; SODIUM CHLORIDE; VANCOMYCIN;

ARTICLE; BIOFILM; CHEMISTRY; DOSE RESPONSE; DRUG EFFECT; OSMOTIC PRESSURE; PHYSIOLOGICAL STRESS; STAPHYLOCOCCUS EPIDERMIDIS; STRUCTURE ACTIVITY RELATION;

ANTI-BACTERIAL AGENTS; BIOFILMS; DOSE-RESPONSE RELATIONSHIP, DRUG; OSMOTIC PRESSURE; SODIUM CHLORIDE; STAPHYLOCOCCUS EPIDERMIDIS; STRESS, PHYSIOLOGICAL; STRUCTURE-ACTIVITY RELATIONSHIP; VANCOMYCIN;

EID: 84879002581     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la401322k     Document Type: Article

References (55)

1. Costerton, J. W.; Stewart, P. S.; Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections Science 1999, 284, 1318
2. Stewart, P. S.; Franklin, M. J. Physiological heterogeneity in biofilms Nat. Rev. Microbiol. 2008, 6, 199-210 (Pubitemid 351256315)
3. Fux, C. A.; Costerton, J. W.; Stewart, P. S.; Stoodley, P. Survival strategies of infectious biofilms Trends Microbiol. 2005, 13, 34-40 (Pubitemid 40082395)
4. Wilking, J. N.; Angelini, T. E.; Seminara, A.; Brenner, M. P.; Weitz, D. A. Biofilms as complex fluids MRS Bull. 2011, 36
5. Zaccarelli, E. Colloidal gels: Equilibrium and non-equilibrium routes J. Phys.: Condens. Matter 2007, 19, 323101
6. Hohne, D. N.; Younger, J. G.; Solomon, M. J. Flexible Microfluidic Device for Mechanical Property Characterization of Soft Viscoelastic Solids Such as Bacterial Biofilms Langmuir 2009, 25, 7743-7751
7. Rogers, S. S.; van, d. W., C.; Waigh, T. A. Microrheology of Bacterial Biofilms In Vitro: Staphylococcus aureus and Pseudomonas aeruginosa Langmuir 2008, 24, 13549-13555
8. Hall-Stoodley, L.; Costerton, J. W.; Stoodley, P. Bacterial biofilms: from the Natural environment to infectious diseases Nat. Rev. Microbiol. 2004, 2, 95-108 (Pubitemid 39490064)
9. Lieleg, O.; Caldara, M.; Baumgärtel, R.; Ribbeck, K. Mechanical robustness of Pseudomonas aeruginosa biofilms Soft Matter 2011, 7, 3307-3314
10. Aggarwal, S.; Poppele, E. H.; Hozalski, R. M. Development and testing of a novel microcantilever technique for measuring the cohesive strength of intact biofilms Biotechnol. Bioeng. 2010, 105, 924-934
11. Dunne, W. M., Jr. Bacterial adhesion: seen any good biofilms lately? Clin. Microbiol. Rev. 2002, 15, 155
12. Xavier, J. B.; White, D. C.; Almeida, J. S. Automated biofilm morphology quantification from confocal laser scanning microscopy imaging Water Sci. Technol. 2003, 47, 31-37 (Pubitemid 36503117)
13. Beyenal, H.; Donovan, C.; Lewandowski, Z.; Harkin, G. Three-dimensional biofilm structure quantification J. Microbiol. Methods 2004, 59, 395-413 (Pubitemid 39370801)
14. Heydorn, A.; Nielsen, A. T.; Hentzer, M.; Sternberg, C.; Givskov, M.; Ersbøll, B. K.; Molin, S. Quantification of biofilm structures by the novel computer program COMSTAT Microbiology 2000, 146, 2395
15. McLean, J. S.; Ona, O. N.; Majors, P. D. Correlated biofilm imaging, transport and metabolism measurements via combined nuclear magnetic resonance and confocal microscopy ISME J. 2007, 2, 121-131 (Pubitemid 351225685)
16. Dzul, S. P.; Thornton, M. M.; Hohne, D. N.; Stewart, E. J.; Shah, A. A.; Bortz, D. M.; Solomon, M. J.; Younger, J. G. Contribution of the Klebsiella pneumoniae Capsule to Bacterial Aggregate and Biofilm Microstructures Appl. Environ. Microbiol. 2011, 77, 1777-1782
17. Berk, V.; Fong, J. C. N.; Dempsey, G. T.; Develioglu, O. N.; Zhuang, X.; Liphardt, J.; Yildiz, F. H.; Chu, S. Molecular Architecture and Assembly Principles of Vibrio cholerae Biofilms Science 2012, 337, 236-239
18. Crocker, J. C.; Grier, D. G. Methods of digital video microscopy for colloidal studies J. Colloid Interface Sci. 1996, 179, 298-310 (Pubitemid 26172272)
19. Dibble, C. J.; Kogan, M.; Solomon, M. J. Structure and dynamics of colloidal depletion gels: Coincidence of transitions and heterogeneity Phys. Rev. E 2006, 74, 041403
20. Poon, W. C. K.; Weeks, E. R.; Royall, C. P. On measuring colloidal volume fractions Soft Matter 2012, 8, 21-30
21. Dill, K. A.; Bromberg, S. Molecular driving forces: statistical thermodynamics in chemistry and biology. 2003.
22. Uçkay, I.; Pittet, D.; Vaudaux, P.; Sax, H.; Lew, D.; Waldvogel, F. Foreign body infections due to Staphylococcus epidermidis Ann. Med. 2009, 41, 109-119
23. Gaboriaud, F.; Gee, M. L.; Strugnell, R.; Duval, J. F. L. Coupled Electrostatic, Hydrodynamic, and Mechanical Properties of Bacterial Interfaces in Aqueous Media Langmuir 2008, 24, 10988-10995
24. Camesano, T. A.; Natan, M. J.; Logan, B. E. Observation of Changes in Bacterial Cell Morphology Using Tapping Mode Atomic Force Microscopy Langmuir 2000, 16, 4563-4572
25. Xu, H.; Murdaugh, A. E.; Chen, W.; Aidala, K. E.; Ferguson, M. A.; Spain, E. M.; Núñez, M. E. Characterizing Pilus-Mediated Adhesion of Biofilm-Forming E. coli to Chemically Diverse Surfaces Using Atomic Force Microscopy Langmuir 2013, 29, 3000-3011
26. Emerson, Bergstrom, T. S.; Liu, Y.; Soto, E. R.; Brown, C. A.; McGimpsey, W. G.; Camesano, T. A. Microscale Correlation between Surface Chemistry, Texture, and the Adhesive Strength of Staphylococcus epidermidis Langmuir 2006, 22, 11311-11321 (Pubitemid 46129676)
27. Busscher, H. J.; van de Belt-Gritter, B.; Dijkstra, R. J. B.; Norde, W.; van, d. M.; Henny, C. Streptococcus mutans and Streptococcus intermedius Adhesion to Fibronectin Films Are Oppositely Influenced by Ionic Strength Langmuir 2008, 24, 10968-10973
28. Pavlovsky, L.; Younger, J. G.; Solomon, M. J. In situ rheology of Staphylococcus epidermidis bacterial biofilms Soft Matter 2013, 9, 122-131
29. Shaw, T.; Winston, M.; Rupp, C. J.; Klapper, I.; Stoodley, P. Commonality of Elastic Relaxation Times in Biofilms Phys. Rev. Lett. 2004, 93, 098102
30. Towler, B. W.; Rupp, C. J.; Cunningham, A. L. B.; Stoodley, P. Viscoelastic Properties of a Mixed Culture Biofilm from Rheometer Creep Analysis Biofouling 2003, 19, 279-285 (Pubitemid 37417792)
31. McMillan, D. E. Hemorheology: Principles and Concepts. In Levin and O'Neal's the Diabetic Foot, 7 th ed.; Bowker, J. H.; Pfeifer, M. A., Eds.; Elsevier: Philadelphia, PA, 2008; Chapter 4, pp 75-88.
32. Howden, L.; Giddings, D.; Power, H.; Aroussi, A.; Vloeberghs, M.; Garnett, M.; Walker, D. Three-dimensional cerebrospinal fluid flow within the human ventricular system Comput. Methods Biomech. Biomed. Eng. 2008, 11, 123-133
33. Lykoudis, P. S.; Roos, R. The fluid mechanics of the ureter from a lubrication theory point of view J. Fluid Mech. 1970, 43, 661-674
34. Christensen, G. D.; Simpson, W. A.; Anglen, J. O.; Gainor, B. J. Methods for Evaluating Attached Bacteria and Biofilms. In Handbook of Bacterial Adhesion; An, Y. H.; Friedman, R. J., Eds.; Humana Press: Totowa, NJ, 2000; pp 213-233.
35. Dobinsky, S.; Kiel, K.; Rohde, H.; Bartscht, K.; Knobloch, J. K.-M.; Horstkotte, M. A.; Mack, D. Glucose-Related Dissociation between icaADBC Transcription and Biofilm Expression by Staphylococcus epidermidis: Evidence for an Additional Factor Required for Polysaccharide Intercellular Adhesin Synthesis J. Bacteriol. 2003, 185, 2879-2886 (Pubitemid 36514599)
36. Stepanović, S.; Vuković, D.; Hola, V.; Bonadventura, G. D.; Djukić, S.; Ćirković, I.; Ruzicka, F. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci APMIS 2007, 115, 891-899 (Pubitemid 47260470)
37. Rachid, S.; Ohlsen, K.; Witte, W.; Hacker, J.; Ziebuhr, W. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis Antimicrob. Agents Chemother. 2000, 44, 3357
38. Conlon, K. M.; Humphreys, H.; O'Gara, J. P. icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis J. Bacteriol. 2002, 184, 4400
39. Polonio, R. E.; Mermel, L. A.; Paquette, G. E.; Sperry, J. F. Eradication of biofilm-forming Staphylococcus epidermidis (RP62A) by a combination of sodium salicylate and vancomycin Antimicrob. Agents Chemother. 2001, 45, 3262
40. Kogan, M.; Dibble, C. J.; Rogers, R. E.; Solomon, M. J. Viscous solvent colloidal system for direct visualization of suspension structure, dynamics and rheology J. Colloid Interface Sci. 2008, 318, 252-263 (Pubitemid 350299386)
41. Lu, P. J.; Zaccarelli, E.; Ciulla, F.; Schofield, A. B.; Sciortino, F.; Weitz, D. A. Gelation of particles with short-range attraction Nature 2008, 453, 499-503 (Pubitemid 351733318)
42. Allen, M. P.; Tildesley, D. J. Computer Simulation of Liquids; Oxford University Press: New York, 1989.
43. Ganesan, M.; Stewart, E. J.; Szafranski, J.; Satorius, A.; Younger, J. G.; Solomon, M. J. Molar mass, entanglement and associations of the biofilm polysaccharide of Staphylococcus epidermidis Biomacromolecules 2013, 14, 1474-1481
44. Dinsmore, A. D.; Prasad, V.; Wong, I. Y.; Weitz, D. A. Microscopic Structure and Elasticity of Weakly Aggregated Colloidal Gels Phys. Rev. Lett. 2006, 96, 185502
45. Lattuada, M.; Wu, H.; Hasmy, A.; Morbidelli, M. Estimation of Fractal Dimension in Colloidal Gels Langmuir 2003, 19, 6312-6316
46. Blaaderen, A. v.; Wiltzius, P. Real-Space Structure of Colloidal Hard-Sphere Glasses Sci. New Ser. 1995, 270, 1177-1179
47. Dinsmore, A. D.; Weeks, E. R.; Prasad, V.; Levitt, A. C.; Weitz, D. A. Three-Dimensional Confocal Microscopy of Colloids Appl. Opt. 2001, 40, 4152-4159
48. Lin, M. Y.; Lindsay, H. M.; Weitz, D. A.; Ball, R. C.; Klein, R.; Meakin, P. Universality in colloid aggregation Nature 1989, 339, 360-362
49. Potanin, A. A. On the Computer Simulation of the Deformation and Breakup of Colloidal Aggregates in Shear Flow J. Colloid Interface Sci. 1993, 157, 399-410
50. Hsiao, L. C.; Newman, R. S.; Glotzer, S. C.; Solomon, M. J. Role of isostaticity and load-bearing microstructure in the elasticity of yielded colloidal gels Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 16029-16034
51. Russel, W. B.; Saville, D. A.; Schowalter, W. R. Colloidal dispersions. 1992.
52. Carpineti, M.; Giglio, M. Spinodal-type dynamics in fractal aggregation of colloidal clusters Phys. Rev. Lett. 1992, 68, 3327-3330
53. Krall, A. H.; Weitz, D. A. Internal Dynamics and Elasticity of Fractal Colloidal Gels Phys. Rev. Lett. 1998, 80, 778-781 (Pubitemid 128623859)
54. Hammond, J. F.; Stewart, E. J.; Younger, J. G.; Solomon, M. J.; Bortz, D. M. Spatially Heterogeneous Biofilm Simulations using an Immersed Boundary Method with Lagrangian Nodes Defined by Bacterial Locations. 2013, arXiv preprint arXiv:1302.3663. arXiv.org e-Print archive. http://arxiv.org/abs/1302. 3663.
55. Mitri, S.; Xavier, J. B.; Foster, K. R. Social evolution in multispecies biofilms Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 10839-10846