Single-cell control of initial spatial structure in biofilm development using laser trapping

Langmuir

Volumn 30, Issue 15, 2014, Pages 4522-4530

  Hutchison, Jaime B ^a   Rodesney, Christopher A ^a   Kaushik, Karishma S ^a   Le, Henry H ^a   Hurwitz, Daniel A ^a   Irie, Yasuhiko ^b   Gordon, Vernita D ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b University of Bath   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFILMS;

BACTERIAL GROWTH; BIOFILM DEVELOPMENT; BIOFILM INFECTIONS; EMBEDDING MATRICES; PSEUDOMONAS AERUGINOSA; SPATIAL STRUCTURE; STAPHYLOCOCCUS AUREUS; SURFACE ADHESION;

BACTERIA;

BACTERIUM ADHERENCE; BIOFILM; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

BACTERIAL ADHESION; BIOFILMS; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

EID: 84899462508     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la500128y     Document Type: Article

References (65)

1. Darouiche, R. Treatment of infections associated with surgical implants New Engl. J. Med. 2004, 350, 1422-1429
2. Perencevich, E.; Sands, K.; Cosgrove, S.; Guadagnoli, E.; Meara, E.; Platt, R. Health and economic impact of surgical site infections diagnosed after hospital discharge Emerging Infect. Dis. 2003, 9, 196-203
3. Ramsey, S.; Newton, K.; Blough, D.; McCulloch, D.; Sandhu, N.; Reiber, G.; Wagner, E. H. Incidence, outcomes, and cost of foot ulcers in patients with diabetes Diabetes Care 1999, 22, 382-387
4. Guelon, T.; Mathias, J.-D.; Deffuant, G. Influence of spatial structure on effective nutrient diffusion in bacterial biofilms J. Biol. Phys. 2012, 38, 573-588
5. Timp, W.; Mirsaidov, U.; Matsudaira, P.; Timp, G. Jamming prokaryotic cell-to-cell communications in a model biofilm Lab Chip 2009, 9, 925-934
6. Meyer, A.; Megerle, J.; Kuttler, C.; Muller, J.; Aquilar, C.; Eberl, L. Dynamics of AHL mediated quorum sensing under flow and non-flow conditions Phys. Biol. 2012, 9, 026007
7. Flickinger, S.; Copeland, M.; Downes, E.; Braasch, A.; Tuson, H.; Eun, Y.-J. Quorum sensing between Pseudomonas aeruginosa biofilms accelerates cell growth J. Am. Chem. Soc. 2011, 133, 5966-5975
8. Dilanji, G.; Langebrake, J.; De Leenher, P.; Hagen, S. Quorum activation at a distance: spatiotemporal patterns of gene regulation from diffusion of an autoinducer signal J. Am. Chem. Soc. 2012, 134, 5618-5626
9. Connell, J.; Wessel, A.; Parsek, M.; Ellington, A.; Whiteley, M.; Shear, J. Probing prokaryotic social behaviors with bacterial lobster traps mBio 2010, 1, e00202-e00210
10. Koley, D.; Ramsey, M.; Bard, A.; Whiteley, M. Discovery of a biofilm electrocline using real-time 3D metabolite analysis Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 19996-20001
11. Tolker-Nielsen, T.; Molin, S. Spatial organization of microbial biofilm communities Microb. Ecol. 2000, 40, 75-84
12. Wessel, A.; Hmelo, L.; Parsek, M.; Whiteley, M. Going local: technologies for exploring bacterial microenvironments Nat. Rev. Microbiol. 2013, 11, 337-348
13. Meyer, A.; Megerle, J.; Muller, C. K. J.; Aguilar, C.; Eberl, L.; Hense, B. Dynamics of AHL mediated quorum sensing under flow and non-flow conditions Phys. Biol. 2012, 9, 026007
14. Gu, H.; Hou, S.; Yongyat, C.; De Tore, S.; Ren, D. Patterned biofilm formation reveals a mechanism for structural heterogeneity in bacterial biofilms Langmuir 2013, 29, 11145-11153
15. Suo, Z.; Avci, R.; Yang, X.; Pascual, D. Efficient immobilization and patterning of live bacterial cells Langmuir 2008, 24, 4161-4167
16. Suo, Z.; Yang, X.; Avci, R.; Deliorman, M.; Rugheimer, P.; Pascual, D.; Idzerda, Y. Antibody selection for immobilizing living bacteria Anal. Chem. 2009, 81, 7571-7578
17. Garnett, J.; Matthews, S. Interactions in bacterial biofilm development: a structural perspective Curr. Protein Pept. Sci. 2012, 13, 739-755
18. Conrad, J. Physics of bacterial near-surface motility using flagella and type IV pili: implications for biofilm formation Res. Microbiol. 2012, 163, 619-629
19. Guvener, Z.; Harwood, C. Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces Mol. Microbiol. 2007, 66, 1459-1473
20. Merritt, J.; Ha, D.-G.; Cowles, K.; Lu, W.; Morales, D.; Rabinowitz, J.; Gitai, Z.; O'Toole, G. A. Specific control of Pseudomonas aeruginosa surface-associated behaviors by two c-di-GMP diguanylate cyclases mBio 2010, 1, e00183
21. Hengge, R. Principles of c-di-GMP signalling in bacteria Nat. Rev. Microbiol. 2009, 7, 263-273
22. Zhang, W.; Sileika, T.; Packman, A. Effects of fluid flow conditions on interactions between species in biofilms FEMS Microbiol. Ecol. 2013, 84, 344-354
23. Dalton, T.; Dowd, S.; Wolcott, R.; Sun, Y.; Watters, C.; Griswold, J.; Rumbaugh, K. P. An in vivo polymicrobial biofilm wound infection model to study interspecies interactions PLoS One 2011, 6, e27317
24. Peters, B.; Jabra-Rizk, M.; O'May, G.; Costerton, J.; Shirtliff, M. Polymicrobial interactions: impact on pathogenesis and human disease Clin. Microbiol. Rev. 2012, 25, 193-213
25. Sibley, C.; Parkins, M.; Rabin, H.; Surette, M. The relevance of the polymicrobial nature of airway infection in the acute and chronic management of patients with cystic fibrosis Curr. Opin. Invest. Drugs 2009, 10, 787-794
26. Kim, H.; Boedicker, J.; Choi, J.; Ismagilov, R. Defined spatial structure stabilizes a synthetic multispecies bacterial community Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 18188-18193
27. Yaguchi, T.; Dwidar, M.; Byun, C.; Leung, B.; Lee, S.; Cho, Y.-K.; Mitchell, R. J.; Takayama, S. Aqueous two-phase system-derived biofilms for bacterial interaction studies Biomacromolecules 2012, 13, 2655-2661
28. Weibel, D.; Lee, A.; Mayer, M.; Brady, S.; Bruzewics, D.; Yang, J.; DiLuzio, W. R.; Clardy, J.; Whitesides, G. M. Bacterial printing press that regenerates its ink: contact-printing bacteria using hydrogel stamps Langmuir 2005, 21, 6436-6442
29. Korgaonkar, A.; Trivedi, U.; Rumbaugh, K.; Whiteley, M. Community surveillance enhances Pseudomonas aeruginosa virulence during polymicrobial infection Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 1059-1064
30. Korgaonkar, A.; Whiteley, M. Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan J. Bacteriol. 2011, 193, 909-917
31. Hoffman, L.; Deziel, E.; D'Argenio, D.; Lepine, F.; Emerson, J.; McNamara, S.; Gibson, R. L.; Ramsey, B. W.; Miller, S. I. Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 19890-19895
32. Goldsworthy, M. Gene expression of Pseudomonas aeruginosa and MRSA within a catheter-associated urinary tract infection biofilm model Biosci. Horiz. 2008, 1, 28-37
33. Duan, K.; Dammel, C.; Stein, J.; Rabin, H.; Surette, M. Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication Mol. Microbiol. 2003, 50, 1477-1491
34. Sibley, C.; Duan, K.; Fischer, C.; Parkins, M.; Storey, D.; Rabin, H.; Surette, M. G. Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections PLoS Pathog. 2008, 4, e1000184
35. Battin, T.; Sloan, W.; Kjelleberg, S.; Daims, H.; Head, I.; Curtis, T.; Eberl, L. Microbial landscapes: new paths to biofilm research Nat. Rev. Microbiol. 2007, 5, 76-81
36. Rogers, G.; Hoffman, L.; Carroll, M.; Bruce, K. Interpreting infective microbiota: the importance of an ecological perspective Trends Microbiol. 2012, 21, 271-276
37. Irie, Y.; Starkey, M.; Edwards, A.; Wozniak, D.; Romeo, T.; Parsek, M. Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA Mol. Microbiol. 2010, 78, 158-172
38. Lambertsen, L.; Sternberg, C.; Molin, S. Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins Environ. Microbiol. 2004, 6, 726-732
39. Davies, D.; Parsek, M.; Pearson, J.; Iglewski, B.; Costerton, J.; Greenberg, E. The involvement of cell-to-cell signals in the development of a bacterial biofilm Science 1998, 280, 295-298
40. Yarwood, J.; Bartels, D.; Volper, E.; Greenberg, E. Quorum sensing in Staphylococcus aureus biofilms J. Bacteriol. 2004, 186, 1838-1850
41. Heydorn, A.; Nielsen, A.; Hentzer, M.; Sternberg, C.; Givskov, M.; Ersboll, B.; Molin, S. Quantification of biofilm structures by the novel computer program COMSTAT Microbiology 2000, 146, 2395-2407
42. Sternberg, C.; Tolker-Nielsen, T. Growing and analyzing biofilms in flow cells Curr. Protocols Microbiol. 2006, 1, 1B.2
43. Ashkin, A. History of optical trapping and manipulation of small-neutral particls, atoms, and molecules IEEE J. Sel. Top. Quantum Electron. 2000, 6, 841-856
44. Woods, D.; Straus, D.; Johanson, W.; Berry, V.; Bass, J. Rolie of pili in adherence of Pseudomonas aeruginosa to mammalian buccal epithelial cells Infect. Immunol. 1980, 26, 1146-1151
45. Doig, P.; Todd, T.; Sastry, P.; Lee, K.; Hodges, R.; Paranchych, W.; Irvin, R. T. Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells Infect. Immunol. 1988, 56, 1641-1646
46. Ashkin, A.; Dziedzic, J. Optical trapping and manipulation of viruses and bacteria Science 1987, 235, 1517-1520
47. Ashkin, A.; Dziedzic, J.; Yamane, T. Optical trapping and manipulation of single cells using infrared laser beams Nature 1987, 330, 769-771
48. Neuman, K.; Chadd, E.; Liou, G.; Bergman, K.; Block, S. Characterization of photodamage to Escherichia coli in optical traps Biophys. J. 1999, 77, 2856-2863
49. Darch, S.; West, S.; Winzer, K.; Diggle, S. Density-dependent fitness benefits in quorum-sensing bacterial populations Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 8259-8263
50. Diggle, S.; Griffin, A.; Campbell, G.; West, S. Cooperation and conflict in quorum-sensing bacterial populations Nature 2007, 450, 411-414
51. Cooley, B.; Thatcher, T.; Hashmi, S.; L'Her, G.; Le, H.; Hurwitz, D. The extracellular polysaccharide Pel makes the attachment of P. aeruginosa to surfaces symmetric and short-ranged Soft Matter 2013, 9, 3871-3876
52. Hendricks, K.; Burd, T.; Anglen, J.; Simpson, A.; Christensen, G.; Gainor, B. Synergy between Staphylococcus aureus and Pseudomonas aeruginosa in a rat model of complex orthopaedic wounds J. Bone Joint Surg. Am. 2001, 83, 855-861
53. Erb-Downward, J.; Thompson, D.; Han, M.; Freeman, C.; McCloskey, L.; Schmidt, L.; Young, V. B.; Toews, G. B.; Curtis, J. L.; Sundaram, B.; Martinez, F. J.; Huffnagle, F. B. Analysis of the lung microbiome in the "healthy" smoker and in COPD PLoS One 2011, 6, e16384
54. Willner, D.; Haynes, M. R.; Furlan, M.; Schmieder, R.; Lim, Y. W.; Rainey, P. B.; Rohwer, F.; Conrad, D. Spatial distribution of microbial communities in the cystic fibrosis lung ISME J. 2012, 6, 471-474
55. Mitchell, G; Malouin, F. Outcome and Prevention of Pseudomonas aeruginosa-Staphylococcus aureus Interactions during Pulmonary Infections in Cystic Fibrosis. In Cystic Fibrosis: Renewed Hopes through Research; Sriramulu, D, Eds.; InTech: Rijeka, Croatia, 2012.
56. Sibley, C.; Surette, M. The polymicrobial nature of airway infections in cystic fibrosis: Cangene gold medal lecture Can. J. Microbiol. 2011, 57, 69-77
57. Gilchrist, F.; Salamat, S.; Clayton, S.; Peach, J.; Alexander, J.; Lenney, W. Bronchoalveolar lavage in children with cystic fibrosis: how many lobes should be sampled? Arch. Dis. Childhood 2011, 96, 215-217
58. Gutierrez, J.; Grimwood, K.; Armstrong, D.; Carlin, J.; Carzino, R.; Olinsky, A.; Robertson, C. F.; Phelan, P. D. Interlobar differences in bronchoalveolar lavage fluid from children with cystic fibrosis Eur. Respir. J. 2001, 17, 281-286
59. Smith, D.; Smith, E.; Pitt, T.; Stableforth, D. Regional microbiology of the cystic fibrosis lung: a post-mortem study in adults J. Infect. 1998, 37, 41-43
60. Rudkjobing, V.; Thomsen, T.; Alhede, M.; Kragh, K.; Nielsen, P.; Johansen, U.; Givskov, M.; Hoiby, N.; Bjarnsholt, T. The microorganisms in chronically infected end-stage and non-end-stage cystic fibrosis patients FEMS Immunol. Med. Microbiol. 2012, 65, 236-244
61. Fazli, M.; Bjarnsholt, T.; Kirketerp-Moller, K.; Jorgensen, B.; Andersen, A.; Krogfelt, K.; Givskov, M.; Tolker-Nielsen, T. Nonrandom distribution of Pseudomonas aeruginosa and Staphylococcus aureus in chronic wounds J. Clin. Microbiol. 2009, 47, 4084-4089
62. Yang, L.; Hengzhuang, W.; Wu, H.; Damkiaer, S.; Jochumsen, N.; Song, Z.; Givskov, M.; Hoiby, N.; Molin, S. Polysaccharides serve as scaffolds of biofilms formed by mucoid Pseudomonas aeruginosa FEMS Immunol. Med. Microbiol. 2012, 65, 366-376
63. Yang, L.; Liu, Y.; Markussen, T.; Hoiby, N.; Tolker-Nielsen, T.; Molin, S. Pattern differentiation in co-culture biofilms formed by Staphylococcus aureus and Pseudomonas aeruginosa FEMS Immunol. Med. Microbiol. 2011, 62, 339-347
64. An, D.; Danhorn, T.; Fuqua, C.; Parsek, M. Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 3828-3833
65. Harrison, F. Microbial ecology of the cystic fibrosis lung Microbiology 2007, 153, 917-923