10.1007/s40204-017-0061-2

Evaluation of the role of substrate and albumin on Pseudomonas aeruginosa biofilm morphology through FESEM and FTIR studies on polymeric biomaterials

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  • S. Dutta Sinha*1,
  • Susmita Chatterjee2,
  • P. K. Maiti2,
  • S. Tarafdar1,
  • S. P. Moulik3,
  1. Department of Physics, Jadavpur University, Kolkata, 700032, IN
  2. Department of Microbiology, SSKM Hospital-Institute of Postgraduate Medical Education and Research, Kolkata, 700020, IN
  3. Centre for Surface Science, Department of Chemistry, Jadavpur University, Kolkata, 700032, IN
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Published in Issue 2017-02-02

How to Cite

Dutta Sinha, S., Chatterjee, S., Maiti, P. K., Tarafdar, S., & Moulik, S. P. (2017). Evaluation of the role of substrate and albumin on Pseudomonas aeruginosa biofilm morphology through FESEM and FTIR studies on polymeric biomaterials. Progress in Biomaterials, 6(1-2 (May 2017). https://doi.org/10.1007/s40204-017-0061-2
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Abstract

Abstract Bacterial biofilms pose the greatest challenge to implant surgeries leading to device-related infections and implant failure. Our present study aims at monitoring the variation in the biofilm architecture of a clinically isolated strain and ATCC 27853 strain of Pseudomonas aeruginosa on two polymeric biomaterials, used in implants. The perspective of our study is to recognize the potential of these two biomaterials to create biofilm infections and develop the understanding regarding their limitations of use and handle patients with this deeper insight. The final goal, however, is an accurate interpretation of substrate-microbe interactions in the two biomaterials, which will provide us the knowledge of possible surface modifications to develop of an efficacious anti-biofilm therapy for deterring implant infections. The reference strain ATCC 27853 and a clinical isolate of P. aeruginosa collected from urinary catheters of patients suffering from urinary tract infections, have been used as microbes while clinical grades of polypropylene and high density polyethylene, have been used as ‘substrates’ for biofilm growth. The variation in the nature of the ‘substrate’ and ‘conditioning layer’ of BSA have been found to affect the biofilm architecture as well as the physiology of the biofilm-forming bacteria, accompanied by an alteration in the nature and volume of EPS (extracellular polysaccharide) matrices. Graphical Abstract

Keywords

  • Biofilms,
  • Biomaterials,
  • Adsorption,
  • Bacteria,
  • Proteins,
  • Conditioning layer
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References

  1. Alava et al. (2013) Control of the graphene–protein interface is required to preserve adsorbed protein function 85(5) (pp. 2754-2759) https://doi.org/10.1021/ac303268z
  2. Almaguer-Flores et al. (2012) Influence of topography and hydrophilicity on initial oral biofilm formation on microstructured titanium surfaces in vitro 23(3) (pp. 301-307) https://doi.org/10.1111/j.1600-0501.2011.02184.x
  3. Alpkvist et al. (2006) Three-dimensional biofilm model with individual cells and continuum EPS matrix 94(5) (pp. 961-979) https://doi.org/10.1002/bit.20917
  4. Amiji and Park (1993) Surface modification of polymeric biomaterials with poly(ethylene oxide), albumin, and heparin for reduced thrombogenicity 4(3) (pp. 217-234) https://doi.org/10.1163/156856293X00537
  5. An and Friedman (1998) Concise review of mechanisms of bacterial adhesion to biomaterial surfaces 43(3) (pp. 338-348) https://doi.org/10.1002/(SICI)1097-4636(199823)43:3<338::AID-JBM16>3.0.CO;2-B
  6. Badihi Hauslich et al. (2013) The adhesion of oral bacteria to modified titanium surfaces: role of plasma proteins and electrostatic forces 24(A100) (pp. 49-56) https://doi.org/10.1111/j.1600-0501.2011.02364.x
  7. Baier (2006) Surface behaviour of biomaterials: the theta surface for biocompatibility 17(11) (pp. 1057-1062) https://doi.org/10.1007/s10856-006-0444-8
  8. Bakker et al. (2003) The effect of dissolved organic carbon on bacterial adhesion to conditioning films adsorbed on glass from natural seawater collected during different seasons 19(6) (pp. 391-407) https://doi.org/10.1080/08927010310001634898
  9. Beal and Betts (2000) Role of rhamnolipid biosurfactants in the uptake and mineralization of hexadecane in Pseudomonas aeruginosa 89(1) (pp. 158-168) https://doi.org/10.1046/j.1365-2672.2000.01104.x
  10. Beyenal and Lewandowski (2000) Combined effect of substrate concentration and flow velocity on effective diffusivity in biofilms 34(2) (pp. 528-538) https://doi.org/10.1016/S0043-1354(99)00147-5
  11. Bhosle et al. (2005) Dynamics of amino acids in the conditioning film developed on glass panels immersed in the surface seawaters of Dona Paula Bay 21(2) (pp. 99-107) https://doi.org/10.1080/08927010500097821
  12. Boulmedais et al. (2004) Polyelectrolyte multilayer films with pegylated polypeptides as a new type of anti-microbial protection for biomaterials 25(11) (pp. 2003-2011) https://doi.org/10.1016/j.biomaterials.2003.08.039
  13. Bowden and Li (1997) Nutritional influences on biofilm development 11(1) (pp. 81-99) https://doi.org/10.1177/08959374970110012101
  14. Branda et al. (2005) Biofilms: the matrix revisited 13(1) (pp. 20-26) https://doi.org/10.1016/j.tim.2004.11.006
  15. Caiazza et al. (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa 187(21) (pp. 7351-7361) https://doi.org/10.1128/JB.187.21.7351-7361.2005
  16. Campa et al. (2012) Springer Science & Business Media
  17. Carvalho I, Henriques M, Carvalho S (2013) New strategies to fight bacterial adhesion. In: Microbial Pathogens and Strategies for Combating them: Science, Technology and Education, Formatex Research Center, p 170–178
  18. Castner and Ratner (2002) Biomedical surface science: foundations to frontiers 500(1) (pp. 28-60) https://doi.org/10.1016/S0039-6028(01)01587-4
  19. Chae et al. (2009) Effect of different substrates on the performance, bacterial diversity, and bacterial viability in microbial fuel cells 100(14) (pp. 3518-3525) https://doi.org/10.1016/j.biortech.2009.02.065
  20. Chang and Merritt (1992) Microbial adherence on poly(methyl methacrylate) (PMMA) surfaces 26(2) (pp. 197-207) https://doi.org/10.1002/jbm.820260206
  21. Chu et al. (2002) Plasma-surface modification of biomaterials 36(5) (pp. 143-206) https://doi.org/10.1016/S0927-796X(02)00004-9
  22. Compere et al. (2001) Kinetics of conditioning layer formation on stainless steel immersed in seawater 17(2) (pp. 129-145) https://doi.org/10.1080/08927010109378472
  23. Costerton et al. (1999) Bacterial biofilms: a common cause of persistent infections 284(5418) (pp. 1318-1322) https://doi.org/10.1126/science.284.5418.1318
  24. Dang and Lovell (2016) Microbial surface colonization and biofilm development in marine environments 80(1) (pp. 91-138) https://doi.org/10.1128/MMBR.00037-15
  25. de Paz et al. (2010) The effects of antimicrobials on endodontic biofilm bacteria 36(1) (pp. 70-77) https://doi.org/10.1016/j.joen.2009.09.017
  26. del Prado et al. (2010) Biofilm formation by Streptococcus pneumoniae strains and effects of human serum albumin, ibuprofen, N-acetyl-l-cysteine, amoxicillin, erythromycin, and levofloxacin 67(4) (pp. 311-318) https://doi.org/10.1016/j.diagmicrobio.2010.03.016
  27. Dewez et al. (1999) Competitive adsorption of proteins: key of the relationship between substratum surface properties and adhesion of epithelial cells 20(6) (pp. 547-559) https://doi.org/10.1016/S0142-9612(98)00207-5
  28. Donlan (2001) Biofilm formation: a clinically relevant microbiological process 33(8) (pp. 1387-1392) https://doi.org/10.1086/322972
  29. Etienne et al. (2005) Antifungal coating by biofunctionalized polyelectrolyte multilayered films 26(33) (pp. 6704-6712) https://doi.org/10.1016/j.biomaterials.2005.04.068
  30. Falkinham et al. (2015) Epidemiology and ecology of opportunistic premise plumbing pathogens: Legionella pneumophila, Mycobacterium avium, and Pseudomonas aeruginosa 123(8) https://doi.org/10.1289/ehp.1408692
  31. Fattinger (2014) Focal molography: coherent microscopic detection of biomolecular interaction 4(3)
  32. Flemming and Wingender (2010) The biofilm matrix 8(9) (pp. 623-633) https://doi.org/10.1038/nrmicro2415
  33. Flemming et al. (2007) The EPS matrix: the “house of biofilm cells” 189(22) (pp. 7945-7947) https://doi.org/10.1128/JB.00858-07
  34. Foster (2005) Immune evasion by staphylococci 3(12) (pp. 948-958) https://doi.org/10.1038/nrmicro1289
  35. Freeman and Lock (1995) The biofilm polysaccharide matrix: a buffer against changing organic substrate supply? 40(2) (pp. 273-278) https://doi.org/10.4319/lo.1995.40.2.0273
  36. Garrett et al. (2008) Bacterial adhesion and biofilms on surfaces 18(9) (pp. 1049-1056) https://doi.org/10.1016/j.pnsc.2008.04.001
  37. Haggag WM (2010) The role of biofilm exopolysaccharides on biocontrol of plant diseases. In: Elnashar M (ed) Biopolymers, InTech, Rijeka, Croatia, p 271–284, ISBN: 978-953-307-109-1
  38. Hetrick and Schoenfisch (2006) Reducing implant-related infections: active release strategies 35(9) (pp. 780-789) https://doi.org/10.1039/b515219b
  39. Hochbaum et al. (2011) Inhibitory effects of d-amino acids on Staphylococcus aureus biofilm development 193(20) (pp. 5616-5622) https://doi.org/10.1128/JB.05534-11
  40. Høiby et al. (2010) Antibiotic resistance of bacterial biofilms 35(4) (pp. 322-332) https://doi.org/10.1016/j.ijantimicag.2009.12.011
  41. Hori and Matsumoto (2010) Bacterial adhesion: from mechanism to control 48(3) (pp. 424-434) https://doi.org/10.1016/j.bej.2009.11.014
  42. Hornef et al. (2002) Bacterial strategies for overcoming host innate and adaptive immune responses 3(11) (pp. 1033-1040) https://doi.org/10.1038/ni1102-1033
  43. Huang et al. (2000) Molecular aspects of muco-and bioadhesion: tethered structures and site-specific surfaces 65(1) (pp. 63-71) https://doi.org/10.1016/S0168-3659(99)00233-3
  44. Ignatova et al. (2006) Combination of electrografting and atom-transfer radical polymerization for making the stainless steel surface antibacterial and protein antiadhesive 22(1) (pp. 255-262) https://doi.org/10.1021/la051954b
  45. Imamura et al. (2008) Adsorption characteristics of various proteins to a titanium surface 106(3) (pp. 273-278) https://doi.org/10.1263/jbb.106.273
  46. Jiao et al. (2010) Characterization of extracellular polymeric substances from acidophilic microbial biofilms 76(9) (pp. 2916-2922) https://doi.org/10.1128/AEM.02289-09
  47. Kiehn and Armstrong (1990) Changes in the spectrum of organisms causing bacteremia and fungemia in immunocompromised patients due to venous access devices 9(12) (pp. 869-872) https://doi.org/10.1007/BF01967501
  48. Kohnen et al. (2003) Development of a long-lasting ventricular catheter impregnated with a combination of antibiotics 24(26) (pp. 4865-4869) https://doi.org/10.1016/S0142-9612(03)00379-X
  49. Kugaprasatham et al. (1992) Effect of turbulence on nitrifying biofilms at non-limiting substrate conditions 26(12) (pp. 1629-1638) https://doi.org/10.1016/0043-1354(92)90162-W
  50. Lee et al. (2005) Heterogeneity of biofilms formed by nonmucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis 43(10) (pp. 5247-5255) https://doi.org/10.1128/JCM.43.10.5247-5255.2005
  51. Leonard and Vroman (1992) Is the Vroman effect of importance in the interaction of blood with artificial materials? 3(1) (pp. 95-107) https://doi.org/10.1163/156856292X00105
  52. Li et al. (2006) Two-level antibacterial coating with both release-killing and contact-killing capabilities 22(24) (pp. 9820-9823) https://doi.org/10.1021/la0622166
  53. Li et al. (2012) Surface contact stimulates the just-in-time deployment of bacterial adhesins 83(1) (pp. 41-51) https://doi.org/10.1111/j.1365-2958.2011.07909.x
  54. Liu et al. (2010) Toward a universal “adhesive nanosheet” for the assembly of multiple nanoparticles based on a protein-induced reduction/decoration of graphene oxide 132(21) (pp. 7279-7281) https://doi.org/10.1021/ja100938r
  55. Lynch and Robertson (2008) Bacterial and fungal biofilm infections (pp. 415-428) https://doi.org/10.1146/annurev.med.59.110106.132000
  56. Mah and O’Toole (2001) Mechanisms of biofilm resistance to antimicrobial agents 9(1) (pp. 34-39) https://doi.org/10.1016/S0966-842X(00)01913-2
  57. Nakanishi et al. (2001) On the adsorption of proteins on solid surfaces, a common but very complicated phenomenon 91(3) (pp. 233-244) https://doi.org/10.1016/S1389-1723(01)80127-4
  58. Oberhardt et al. (2008) Genome-scale metabolic network analysis of the opportunistic pathogen Pseudomonas aeruginosa PAO1 190(8) (pp. 2790-2803) https://doi.org/10.1128/JB.01583-07
  59. Peyton (1996) Effects of shear stress and substrate loading rate on Pseudomonas aeruginosa biofilm thickness and density 30(1) (pp. 29-36) https://doi.org/10.1016/0043-1354(95)00110-7
  60. Rios et al. (2007) The effect of polymer surface on the wetting and adhesion of liquid systems 21(3–4) (pp. 227-241) https://doi.org/10.1163/156856107780684567
  61. Roy-Burman et al. (2001) Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections 183(12) (pp. 1767-1774) https://doi.org/10.1086/320737
  62. Rudra et al. (2006) Antimicrobial polypeptide multilayer nanocoatings 17(11) (pp. 1301-1315) https://doi.org/10.1163/156856206778667433
  63. Salta et al. (2013) Marine biofilms on artificial surfaces: structure and dynamics 15(11) (pp. 2879-2893) https://doi.org/10.1111/1462-2920.12186
  64. Saygun et al. (2006) Gold and gold-palladium coated polypropylene grafts in a S. epidermidis wound infection model 131(1) (pp. 73-79) https://doi.org/10.1016/j.jss.2005.06.020
  65. Stewart and Costerton (2001) Antibiotic resistance of bacteria in biofilms 358(9276) (pp. 135-138) https://doi.org/10.1016/S0140-6736(01)05321-1
  66. Stoodley P, Boyle JD, Dodds I, Lappin-Scott HM (1997) Consensus model of biofilm structure. In: Wimpenny JWT, Handley PS, Gilbert P, Lappin-Scott HM, Jones M (eds) Biofilms: community interactions and controls, BioLine, Cardiff, U.K, p 1–9
  67. Tang et al. (2010) Influence of substrates on nitrogen removal performance and microbiology of anaerobic ammonium oxidation by operating two UASB reactors fed with different substrate levels 181(1) (pp. 19-26) https://doi.org/10.1016/j.jhazmat.2010.04.015
  68. Tiller et al. (2002) Polymer surfaces derivatized with poly(vinyl-N-hexylpyridinium) kill airborne and waterborne bacteria 79(4) (pp. 465-471) https://doi.org/10.1002/bit.10299
  69. Tuson and Weibel (2013) Bacteria–surface interactions 9(17) (pp. 4368-4380) https://doi.org/10.1039/c3sm27705d
  70. van Oss (1997) Hydrophobicity and hydrophilicity of biosurfaces 2(5) (pp. 503-512) https://doi.org/10.1016/S1359-0294(97)80099-4
  71. van Oss and Good (1991) Surface enthalpy and entropy and the physico-chemical nature of hydrophobic and hydrophilic interactions 12(3–4) (pp. 273-287) https://doi.org/10.1080/01932699108913130
  72. Vo-Dinh (2014) CRC Press
  73. Vogler (2012) Protein adsorption in three dimensions 33(5) (pp. 1201-1237) https://doi.org/10.1016/j.biomaterials.2011.10.059
  74. von Eiff et al. (2005) Infections associated with medical devices 65(2) (pp. 179-214) https://doi.org/10.2165/00003495-200565020-00003
  75. Vu et al. (2009) Bacterial extracellular polysaccharides involved in biofilm formation 14(7) (pp. 2535-2554) https://doi.org/10.3390/molecules14072535
  76. Waldvogel and Bisno (2000) ASM Press
  77. Weinstein and Darouiche (2001) Device-associated infections: a macroproblem that starts with microadherence 33(9) (pp. 1567-1572) https://doi.org/10.1086/323130
  78. Whiteley et al. (2001) Gene expression in Pseudomonas aeruginosa biofilms 413(6858) (pp. 860-864) https://doi.org/10.1038/35101627
  79. Wimpenny and Colasanti (1997) A unifying hypothesis for the structure of microbial biofilms based on cellular automaton models 22(1) (pp. 1-16) https://doi.org/10.1111/j.1574-6941.1997.tb00351.x
  80. Wingender et al. (2012) Springer Science & Business Media
  81. Zhang et al. (1999) Comparison of extraction methods for quantifying extracellular polymers in biofilms 39(7) (pp. 211-218) https://doi.org/10.1016/S0273-1223(99)00170-5
  82. Zhu et al. (2004) Effect of substrate Henry’s constant on biofilter performance 54(4) (pp. 409-418) https://doi.org/10.1080/10473289.2004.10470918