1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

New Technologies for Studying Biofilms

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • HTML
    226.33 Kb
  • XML
    249.75 Kb
  • PDF
    686.98 Kb
  • Authors: Michael J. Franklin1, Connie Chang3, Tatsuya Akiyama5, Brian Bothner7
  • Editors: Mahmoud Ghannoum9, Matthew Parsek10, Marvin Whiteley11, Pranab Mukherjee12
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Center for Biofilm Engineering, Montana State University-Bozeman, Bozeman, MT 59717; 2: Department of Microbiology and Immunology, Montana State University-Bozeman, Bozeman, MT 59717; 3: Center for Biofilm Engineering, Montana State University-Bozeman, Bozeman, MT 59717; 4: Department of Chemical and Biological Engineering, Montana State University-Bozeman, Bozeman, MT 59717; 5: Center for Biofilm Engineering, Montana State University-Bozeman, Bozeman, MT 59717; 6: Department of Microbiology and Immunology, Montana State University-Bozeman, Bozeman, MT 59717; 7: Center for Biofilm Engineering, Montana State University-Bozeman, Bozeman, MT 59717; 8: Department of Chemistry and Biochemistry, Montana State University-Bozeman, Bozeman, MT 59717; 9: Case Western Reserve University, Cleveland, OH; 10: University of Washington, Seattle, WA; 11: University of Texas at Austin, Austin, TX; 12: Case Western Reserve University, Cleveland, OH
    • Source: microbiolspec August 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0016-2014
  • Received 30 December 2014 Accepted 17 February 2015 Published 21 August 2015
  • Michael J. Franklin, [email protected]
image of New Technologies for Studying Biofilms
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    New Technologies for Studying Biofilms, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/3/4/MB-0016-2014-1.gif /docserver/preview/fulltext/microbiolspec/3/4/MB-0016-2014-2.gif

  • Abstract:

    Bacteria have traditionally been studied as single-cell organisms. In laboratory settings, aerobic bacteria are usually cultured in aerated flasks, where the cells are considered essentially homogenous. However, in many natural environments, bacteria and other microorganisms grow in mixed communities, often associated with surfaces. Biofilms are comprised of surface-associated microorganisms, their extracellular matrix material, and environmental chemicals that have adsorbed to the bacteria or their matrix material. While this definition of a biofilm is fairly simple, biofilms are complex and dynamic. Our understanding of the activities of individual biofilm cells and whole biofilm systems has developed rapidly, due in part to advances in molecular, analytical, and imaging tools and the miniaturization of tools designed to characterize biofilms at the enzyme level, cellular level, and systems level.

  • Citation: Franklin M, Chang C, Akiyama T, Bothner B. 2015. New Technologies for Studying Biofilms. Microbiol Spectrum 3(4):MB-0016-2014. doi:10.1128/microbiolspec.MB-0016-2014.

References

1. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel NC, Dosgupton M, Marine IJ. 1987. Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–461. [PubMed][CrossRef]
2. Costerton JW, Lewandovski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995. Microbial biofilms. Annu Rev Microbiol 49:711–745. [PubMed][CrossRef]
3. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322. [PubMed][CrossRef]
4. Flemming HC, Wingender J. 2010. The biofilm matrix. Nat Rev 8:623–633. [PubMed][CrossRef]
5. Hung C, Zhou Y, Pinkner JS, Dodson KW, Crowley JR, Heuser J, Chapman MR, Hadjifrangiskou M, Henderson JP, Hultgren SJ. 2013. Escherichia coli biofilms have an organized and complex extracellular matrix structure. MBio 4:e00645-00613. doi:10.1128/mBio.00645-13. [PubMed][CrossRef]
6. Soto GE, Hultgren SJ. 1999. Bacterial adhesins: common themes and variations in architecture and assembly. J Bacteriol 181:1059–1071. [PubMed]
7. Fux CA, Costerton JW, Stewart PS, Stoodley P. 2005. Survival strategies of infectious biofilms. Trends Microbiol 13:34–40. [PubMed][CrossRef]
8. Singh R, Ray P, Das A, Sharma M. 2009. Role of persisters and small-colony variants in antibiotic resistance of planktonic and biofilm-associated Staphylococcus aureus: an in vitro study. J Med Microbiol 58:1067–1073. [PubMed][CrossRef]
9. van de Mortel M, Halverson LJ. 2004. Cell envelope components contributing to biofilm growth and survival of Pseudomonas putida in low-water-content habitats. Mol Microbiol 52:735–750. [PubMed][CrossRef]
10. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298. [PubMed][CrossRef]
11. De Kievit TR, Iglewski BH. 1999. Quorum sensing, gene expression, and Pseudomonas biofilms. Methods Enzymol 310:117–128. [PubMed][CrossRef]
12. Fuqua WC, Winans SC, Greenberg EP. 1994. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275. [PubMed]
13. Parsek MR, Greenberg EP. 1999. Quorum sensing signals in development of Pseudomonas aeruginosa biofilms. Methods Enzymol 310:43–55. [PubMed][CrossRef]
14. Parsek MR, Greenberg EP. 2000. Acyl-homoserine lactone quorum sensing in Gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc Natl Acad Sci USA 97:8789–8793. [PubMed][CrossRef]
15. Passador L, Iglewski BH. 1995. Quorum sensing and virulence gene regulation in Pseudomonas aeruginosa, p 65–78. In Roth JA et al. (ed), Virulence Mechanisms of Bacterial Pathogens. American Society for Microbiology, Washington D.C.
16. Pesci EC, Pearson JP, Seed PC, Iglewski BH. 1997. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127–3132. [PubMed]
17. Ueda A, Wood TK. 2009. Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 5:e1000483. doi:10.1371/journal.ppat.1000483. [PubMed][CrossRef]
18. Whiteley M, Lee KM, Greenberg EP. 1999. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96:13904–13909. [PubMed][CrossRef]
19. Zhu J, Mekalanos JJ. 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell 5:647–656. [PubMed][CrossRef]
20. Brint JM, Ohman DE. 1995. Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J Bacteriol 177:7155–7163. [PubMed]
21. Pearson JP, Pesci EC, Iglewski BH. 1997. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179:5756–5767. [PubMed]
22. Tielen P, Rosenau F, Wilhelm S, Jaeger KE, Flemming HC, Wingender J. 2010. Extracellular enzymes affect biofilm formation of mucoid Pseudomonas aeruginosa. Microbiology 156:2239–2252. [PubMed][CrossRef]
23. Glessner A, Smith RS, Iglewski BH, Robinson JA. 1999. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of twitching motility. J Bacteriol 181:1623–1629. [PubMed]
24. Heydorn A, Ersboll B, Kato J, Hentzer M, Parsek MR, Tolker-Nielsen T, Givskov M, Molin S. 2002. Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression. Appl Environ Microbiol 68:2008–2017. [PubMed][CrossRef]
25. Heurlier K, Williams F, Heeb S, Dormond C, Pessi G, Singer D, Camara M, Williams P, Haas D. 2004. Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 186:2936–2945. [PubMed][CrossRef]
26. O’Toole GA, Kolter R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304. [PubMed][CrossRef]
27. Shrout JD, Chopp DL, Just CL, Hentzer M, Givskov M, Parsek MR. 2006. The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol Microbiol 62:1264–1277. [PubMed][CrossRef]
28. Wang Q, Frye JG, McClelland M, Harshey RM. 2004. Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes. Mol Microbiol 52:169–187. [PubMed][CrossRef]
29. Aguilar C, Vlamakis H, Losick R, Kolter R. 2007. Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol 10:638–643. [PubMed][CrossRef]
30. Basler M, Ho BT, Mekalanos JJ. 2013. Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152:884–894. [PubMed][CrossRef]
31. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ. 2012. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483:182–186. [PubMed][CrossRef]
32. Gibbs KA, Urbanowski ML, Greenberg EP. 2008. Genetic determinants of self identity and social recognition in bacteria. Science 321:256–259. [PubMed][CrossRef]
33. Moscoso JA, Mikkelsen H, Heeb S, Williams P, Filloux A. 2011. The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environ Microbiol 13:3128–3138. [PubMed][CrossRef]
34. Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat Rev 6:199–210. [PubMed][CrossRef]
35. Becraft ED, Cohan FM, Kuhl M, Jensen SI, Ward DM. 2011. Fine-scale distribution patterns of Synechococcus ecological diversity in microbial mats of Mushroom Spring, Yellowstone National Park. Appl Environ Microbiol 77:7689–7697. [PubMed][CrossRef]
36. Kim W, Racimo F, Schluter J, Levy SB, Foster KR. 2014. Importance of positioning for microbial evolution. Proc Natl Acad Sci USA 111:E1639–E1647. [PubMed][CrossRef]
37. Ramsing NB, Ferris MJ, Ward DM. 2000. Highly ordered vertical structure of Synechococcus populations within the one-millimeter-thick photic zone of a hot spring cyanobacterial mat. Appl Environ Microbiol 66:1038–1049. [PubMed][CrossRef]
38. Rani SA, Pitts B, Beyenal H, Veluchamy RA, Lewandowski Z, Davison WM, Buckingham-Meyer K, Stewart PS. 2007. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol 189:4223–4233. [PubMed][CrossRef]
39. Rasmussen K, Lewandowski Z. 1998. Microelectrode measurements of local mass transport rates in heterogeneous biofilms. Biotechnol Bioeng 59:302–309. [PubMed][CrossRef]
40. Werner E, Roe F, Bugnicourt A, Franklin MJ, Heydorn A, Molin S, Pitts B, Stewart PS. 2004. Stratified growth in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 70:6188–6196. [PubMed][CrossRef]
41. Boles BR, Thoendel M, Singh PK. 2004. Self-generated diversity produces “insurance effects” in biofilm communities. Proc Natl Acad Sci USA 101:16630–16635. [PubMed][CrossRef]
42. Hansen SK, Rainey PB, Haagensen JA, Molin S. 2007. Evolution of species interactions in a biofilm community. Nature 445:533–536. [PubMed][CrossRef]
43. Allegrucci M, Sauer K. 2007. Characterization of colony morphology variants isolated from Streptococcus pneumoniae biofilms. J Bacteriol 189:2030–2038. [PubMed][CrossRef]
44. Hansen SK, Haagensen JA, Gjermansen M, Jorgensen TM, Tolker-Nielsen T, Molin S. 2007. Characterization of a Pseudomonas putida rough variant evolved in a mixed-species biofilm with Acinetobacter sp. strain C6. J Bacteriol 189:4932–4943. [PubMed][CrossRef]
45. Kirisits MJ, Prost L, Starkey M, Parsek MR. 2005. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71:4809–4821. [PubMed][CrossRef]
46. McEllistrem MC, Ransford JV, Khan SA. 2007. Characterization of in vitro biofilm-associated pneumococcal phase variants of a clinically relevant serotype 3 clone. J Clin Microbiol 45:97–101. [PubMed][CrossRef]
47. Valle J, Vergara-Irigaray M, Merino N, Penades JR, Lasa I. 2007. sigmaB regulates IS256-mediated Staphylococcus aureus biofilm phenotypic variation. J Bacteriol 189:2886–2896. [PubMed][CrossRef]
48. Baty AM, 3rd, Eastburn CC, Diwu Z, Techkarnjanaruk S, Goodman AE, Geesey GG. 2000. Differentiation of chitinase-active and non-chitinase-active subpopulations of a marine bacterium during chitin degradation. Appl Environ Microbiol 66:3566–3573. [PubMed][CrossRef]
49. Baty AM, 3rd, Eastburn CC, Techkarnjanaruk S, Goodman AE, Geesey GG. 2000. Spatial and temporal variations in chitinolytic gene expression and bacterial biomass production during chitin degradation. Appl Environ Microbiol 66:3574–3585. [PubMed][CrossRef]
50. Vlamakis H, Aguilar C, Losick R, Kolter R. 2008. Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev 22:945–953. [PubMed][CrossRef]
51. Gelens L, Hill L, Vandervelde A, Danckaert J, Loris R. 2013. A general model for toxin-antitoxin module dynamics can explain persister cell formation in E. coli. PLoS Comput Biol 9:e1003190. doi:10.1371/journal.pcbi.1003190. [PubMed]
52. Koh RS, Dunlop MJ. 2012. Modeling suggests that gene circuit architecture controls phenotypic variability in a bacterial persistence network. BMC Syst Biol 6:47. [PubMed][CrossRef]
53. Lewis K. 2007. Persister cells, dormancy and infectious disease. Nat Rev 5:48–56. [PubMed][CrossRef]
54. Mulcahy LR, Burns JL, Lory S, Lewis K. 2010. Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J Bacteriol 192:6191–6199. [PubMed][CrossRef]
55. Denef VJ, Mueller RS, Banfield JF. 2010. AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J 4:599–610. [PubMed][CrossRef]
56. Grzymski JJ, Murray AE, Campbell BJ, Kaplarevic M, Gao GR, Lee C, Daniel R, Ghadiri A, Feldman RA, Cary SC. 2008. Metagenome analysis of an extreme microbial symbiosis reveals eurythermal adaptation and metabolic flexibility. Proc Natl Acad Sci USA 105:17516–17521. [PubMed][CrossRef]
57. Inskeep WP, Rusch DB, Jay ZJ, Herrgard MJ, Kozubal MA, Richardson TH, Macur RE, Hamamura N, Jennings R, Fouke BW, Reysenbach AL, Roberto F, Young M, Schwartz A, Boyd ES, Badger JH, Mathur EJ, Ortmann AC, Bateson M, Geesey G, Frazier M. 2010. Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. PLoS One 5:e9773. doi:10.1371/journal.pone.0009773. [CrossRef]
58. Xu P, Gunsolley J. 2014. Application of metagenomics in understanding oral health and disease. Virulence 5:424–432. [PubMed][CrossRef]
59. Ishii S, Suzuki S, Norden-Krichmar TM, Tenney A, Chain PS, Scholz MB, Nealson KH, Bretschger O. 2013. A novel metatranscriptomic approach to identify gene expression dynamics during extracellular electron transfer. Nat Commun 4:1601. [PubMed][CrossRef]
60. Folsom JP, Richards L, Pitts B, Roe F, Ehrlich GD, Parker A, Mazurie A, Stewart PS. 2010. Physiology of Pseudomonas aeruginosa in biofilms as revealed by transcriptome analysis. BMC Microbiol 10:294. [PubMed][CrossRef]
61. Lenz AP, Williamson KS, Pitts B, Stewart PS, Franklin MJ. 2008. Localized gene expression in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 74:4463–4471. [PubMed][CrossRef]
62. 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. [PubMed][CrossRef]
63. Beale DJ, Barratt R, Marlow DR, Dunn MS, Palombo EA, Morrison PD, Key C. 2013. Application of metabolomics to understanding biofilms in water distribution systems: a pilot study. Biofouling 29:283–294. [PubMed][CrossRef]
64. Secor PR, Jennings LK, James GA, Kirker KR, Pulcini ED, McInnerney K, Gerlach R, Livinghouse T, Hilmer JK, Bothner B, Fleckman P, Olerud JE, Stewart PS. 2013. Phevalin (aureusimine B) production by Staphylococcus aureus biofilm and impacts on human keratinocyte gene expression. PLoS One 7:e40973. doi:10.1371/journal.pone.0040973. [PubMed][CrossRef]
65. Klayman BJ, Klapper I, Stewart PS, Camper AK. 2008. Measurements of accumulation and displacement at the single cell cluster level in Pseudomonas aeruginosa biofilms. Environ Microbiol 10:2344–2354. [PubMed][CrossRef]
66. Lam AJ, St-Pierre F, Gong Y, Marshall JD, Cranfill PJ, Baird MA, McKeown MR, Wiedenmann J, Davidson MW, Schnitzer MJ, Tsien RY, Lin MZ. 2012. Improving FRET dynamic range with bright green and red fluorescent proteins. Nat Methods 9:1005–1012. [PubMed][CrossRef]
67. Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, Davidson MW, Tsien RY. 2008. Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods 5:545–551. [PubMed][CrossRef]
68. Shaner NC, Steinbach PA, Tsien RY. 2005. A guide to choosing fluorescent proteins. Nat Methods 2:905–909. [PubMed][CrossRef]
69. McLoon AL, Kolodkin-Gal I, Rubinstein SM, Kolter R, Losick R. 2011. Spatial regulation of histidine kinases governing biofilm formation in Bacillus subtilis. J Bacteriol 193:679–685. [PubMed][CrossRef]
70. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, Molin S, Givskov M, Tolker-Nielsen T. 2006. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59:1114–1128. [PubMed][CrossRef]
71. Baird FJ, Wadsworth MP, Hill JE. 2012. Evaluation and optimization of multiple fluorophore analysis of a Pseudomonas aeruginosa biofilm. J Microbiol Methods 90:192–196. [PubMed][CrossRef]
72. Chen MY, Lee DJ, Tay JH, Show KY. 2007. Staining of extracellular polymeric substances and cells in bioaggregates. Appl Microbiol Biotechnol 75:467–474. [PubMed][CrossRef]
73. Gloag ES, Turnbull L, Huang A, Vallotton P, Wang H, Nolan LM, Mililli L, Hunt C, Lu J, Osvath SR, Monahan LG, Cavaliere R, Charles IG, Wand MP, Gee ML, Prabhakar R, Whitchurch CB. 2013. Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc Natl Acad Sci USA 110:11541–11546. [PubMed][CrossRef]
74. Amann R, Ludwig W. 2000. Ribosomal RNA-targeted nucleic acid probes for studies in microbial ecology. FEMS Microbiol Rev 24:555–565. [PubMed][CrossRef]
75. Brileya KA, Camilleri LB, Fields MW. 2014. 3D-fluorescence in situ hybridization of intact, anaerobic biofilm. Methods Mol Biol 1151:189–197. [PubMed][CrossRef]
76. DeLong EF, Wickham GS, Pace NR. 1989. Phylogenetic stains: ribosomal RNA-based probes for the identification of single cells. Science 243:1360–1363. [PubMed][CrossRef]
77. Moller S, Pedersen AR, Poulsen LK, Arvin E, Molin S. 1996. Activity and three-dimensional distribution of toluene-degrading Pseudomonas putida in a multispecies biofilm assessed by quantitative in situ hybridization and scanning confocal laser microscopy. Appl Environ Microbiol 62:4632–4640. [PubMed]
78. Schramm A, De Beer D, Wagner M, Amann R. 1998. Identification and activities in situ of Nitrosospira and Nitrospira spp. as dominant populations in a nitrifying fluidized bed reactor. Appl Environ Microbiol 64:3480–3485. [PubMed]
79. Hornemann JA, Codd SL, Fell RJ, Stewart PS, Seymour JD. 2009. Secondary flow mixing due to biofilm growth in capillaries of varying dimensions. Biotechnol Bioeng 103:353–360. [PubMed][CrossRef]
80. Hornemann JA, Lysova AA, Codd SL, Seymour JD, Busse SC, Stewart PS, Brown JR. 2008. Biopolymer and water dynamics in microbial biofilm extracellular polymeric substance. Biomacromolecules 9:2322–2328. [PubMed][CrossRef]
81. O’Toole GA, Kolter R. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28:449–461. [PubMed][CrossRef]
82. Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A. 1999. The Calgary biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771–1776. [PubMed]
83. Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R. 2001. Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98:11621–11626. [PubMed][CrossRef]
84. Chimileski S, Franklin MJ, Papke RT. 2014. Biofilms formed by the archaeon Haloferax volcanii exhibit cellular differentiation and social motility, and facilitate horizontal gene transfer. BMC Biol 12:65. [PubMed][CrossRef]
85. Wentland E, Stewart PS, Huang C-T, McFeters GA. 1996. Spatial variations in growth rate within Klebsiella pneumoniae colonies and biofilm. Biotechnol Prog 12:316–321. [PubMed][CrossRef]
86. Huang C, McFeters G, Stewart P. 1996. Evaluation of physiological staining, cryoembedding, and autofluorescence quenching techniques on fouling biofilms. Biofouling 9:269–277. [CrossRef]
87. Anderl JN, Franklin MJ, Stewart PS. 2000. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 44:1818–1824. [PubMed][CrossRef]
88. Goeres DM, Loetterle LR, Hamilton MA, Murga R, Kirby DW, Donlan RM. 2005. Statistical assessment of a laboratory method for growing biofilms. Microbiology 151:757–762. [PubMed][CrossRef]
89. Goeres DM, Hamilton MA, Beck NA, Buckingham-Meyer K, Hilyard JD, Loetterle LR, Lorenz LA, Walker DK, Stewart PS. 2009. A method for growing a biofilm under low shear at the air-liquid interface using the drip flow biofilm reactor. Nat Protoc 4:783–788. [PubMed][CrossRef]
90. Lawrence JR, Korber DR, Hoyle BD, Costerton JW, Caldwell DE. 1991. Optical sectioning of microbial biofilms. J Bacteriol 173:6558–6567. [PubMed]
91. Nivens DE, Ohman DE, Williams J, Franklin MJ. 2001. Role of alginate and its O acetylation in formation of Pseudomonas aeruginosa microcolonies and biofilms. J Bacteriol 183:1047–1057. [PubMed][CrossRef]
92. Stapper AP, Narasimhan G, Ohman DE, Barakat J, Hentzer M, Molin S, Kharazmi A, Hoiby N, Mathee K. 2004. Alginate production affects Pseudomonas aeruginosa biofilm development and architecture, but is not essential for biofilm formation. J Med Microbiol 53:679–690. [PubMed][CrossRef]
93. Xu KD, Franklin MJ, Park CH, McFeters GA, Stewart PS. 2001. Gene expression and protein levels of the stationary phase sigma factor, RpoS, in continuously-fed Pseudomonas aeruginosa biofilms. FEMS Microbiol Lett 199:67–71. [PubMed][CrossRef]
94. Lewandowski Z, Beyenal H. 2001. Limiting-current-type microelectrodes for quantifying mass transport dynamics in biofilms. Methods Enzymol 337:339–359. [PubMed][CrossRef]
95. Dunsmore BC, Jacobsen A, Hall-Stoodley L, Bass CJ, Lappin-Scott HM, Stoodley P. 2002. The influence of fluid shear on the structure and material properties of sulphate-reducing bacterial biofilms. J Ind Microbiol Biotechnol 29:347–353. [PubMed][CrossRef]
96. Rani SA, Pitts B, Stewart PS. 2005. Rapid diffusion of fluorescent tracers into Staphylococcus epidermidis biofilms visualized by time lapse microscopy. Antimicrob Agents Chemother 49:728–732. [PubMed][CrossRef]
97. Xi C, Marks D, Schlachter S, Luo W, Boppart SA. 2006. High-resolution three-dimensional imaging of biofilm development using optical coherence tomography. J Biomed Opt 11:34001. [PubMed][CrossRef]
98. Sackmann EK, Fulton AL, Beebe DJ. 2014. The present and future role of microfluidics in biomedical research. Nature 507:181–189. [PubMed][CrossRef]
99. Groisman A, Lobo C, Cho H, Campbell JK, Dufour YS, Stevens AM, Levchenko A. 2005. A microfluidic chemostat for experiments with bacterial and yeast cells. Nature Methods 2:685–689. [PubMed][CrossRef]
100. Leung K, Zahn H, Leaver T, Konwar KM, Hanson NW, Pagé AP, Lo C-C, Chain PS, Hallam SJ, Hansen CL. 2012. A programmable droplet-based microfluidic device applied to multiparameter analysis of single microbes and microbial communities. Proc Natl Acad Sci USA 109:7665–7670. [PubMed][CrossRef]
101. Locke JC, Elowitz MB. 2009. Using movies to analyse gene circuit dynamics in single cells. Nat Rev Microbiol 7:383–392. [PubMed][CrossRef]
102. Nichols D, Cahoon N, Trakhtenberg E, Pham L, Mehta A, Belanger A, Kanigan T, Lewis K, Epstein S. 2010. Use of ichip for high-throughput in situ cultivation of “uncultivable” microbial species. Appl Environ Microbiol 76:2445–2450. [PubMed][CrossRef]
103. Weibel DB, DiLuzio WR, Whitesides GM. 2007. Microfabrication meets microbiology. Nat Rev Microbiol 5:209–218. [PubMed][CrossRef]
104. Wessel AK, Hmelo L, Parsek MR, Whiteley M. 2013. Going local: technologies for exploring bacterial microenvironments. Nat Rev Microbiol 11:337–348. [PubMed][CrossRef]
105. Boedicker JQ, Li L, Kline TR, Ismagilov RF. 2008. Detecting bacteria and determining their susceptibility to antibiotics by stochastic confinement in nanoliter droplets using plug-based microfluidics. Lab Chip 8:1265–1272. [PubMed][CrossRef]
106. Zhang Q, Lambert G, Liao D, Kim H, Robin K, Tung C-K, Pourmand N, Austin RH. 2011. Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science 333:1764–1767. [PubMed][CrossRef]
107. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. 2004. Bacterial persistence as a phenotypic switch. Science 305:1622–1625. [PubMed][CrossRef]
108. Gefen O, Gabay C, Mumcuoglu M, Engel G, Balaban NQ. 2008. Single-cell protein induction dynamics reveals a period of vulnerability to antibiotics in persister bacteria. Proc Natl Acad Sci USA 105:6145–6149. [PubMed][CrossRef]
109. Boedicker JQ, Vincent ME, Ismagilov RF. 2009. Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals Its variability. Angew Chem Int Ed Engl 48:5908–5911. [PubMed][CrossRef]
110. Balagaddé FK, You L, Hansen CL, Arnold FH, Quake SR. 2005. Long-term monitoring of bacteria undergoing programmed population control in a microchemostat. Science 309:137–140. [PubMed][CrossRef]
111. Rowat AC, Bird JC, Agresti JJ, Rando OJ, Weitz DA. 2009. Tracking lineages of single cells in lines using a microfluidic device. Proc Natl Acad Sci USA 106:18149–18154. [PubMed][CrossRef]
112. Wang P, Robert L, Pelletier J, Dang WL, Taddei F, Wright A, Jun S. 2010. Robust growth of Escherichia coli. Curr Biol 20:1099–1103. [PubMed][CrossRef]
113. Ottesen EA, Hong JW, Quake SR, Leadbetter JR. 2006. Microfluidic digital PCR enables multigene analysis of individual environmental bacteria. Science 314:1464–1467. [PubMed][CrossRef]
114. Baret J-C, Miller OJ, Taly V, Ryckelynck M, El-Harrak A, Frenz L, Rick C, Samuels ML, Hutchison JB, Agresti JJ. 2009. Fluorescence-activated droplet sorting (FADS): efficient microfluidic cell sorting based on enzymatic activity. Lab Chip 9:1850–1858. [PubMed][CrossRef]
115. Gomez-Sjoberg R, Morisette DT, Bashir R. 2005. Impedance microbiology-on-a-chip: microfluidic bioprocessor for rapid detection of bacterial metabolism. J Microelectromechanic Syst 14:829–838. [CrossRef]
116. Mach AJ, Di Carlo D. 2010. Continuous scalable blood filtration device using inertial microfluidics. Biotechnol Bioeng 107:302–311. [PubMed][CrossRef]
117. Wu Z, Willing B, Bjerketorp J, Jansson JK, Hjort K. 2009. Soft inertial microfluidics for high throughput separation of bacteria from human blood cells. Lab Chip 9:1193–1199. [PubMed][CrossRef]
118. Mao H, Cremer PS, Manson MD. 2003. A sensitive, versatile microfluidic assay for bacterial chemotaxis. Proc Natl Acad Sci USA 100:5449–5454. [PubMed][CrossRef]
119. Stocker R, Seymour JR, Samadani A, Hunt DE, Polz MF. 2008. Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc Natl Acad Sci USA 105:4209–4214. [PubMed][CrossRef]
120. Connell JL, Wessel AK, Parsek MR, Ellington AD, Whiteley M, Shear JB. 2010. Probing prokaryotic social behaviors with bacterial “lobster traps.” MBio 1:e00202-00210. doi:10.1128/mBio.00202-10. [PubMed][CrossRef]
121. Eun Y-J, Weibel DB. 2009. Fabrication of microbial biofilm arrays by geometric control of cell adhesion. Langmuir 25:4643–4654. [PubMed][CrossRef]
122. Kim KP, Kim Y-G, Choi C-H, Kim H-E, Lee S-H, Chang W-S, Lee C-S. 2010. In situ monitoring of antibiotic susceptibility of bacterial biofilms in a microfluidic device. Lab Chip 10:3296–3299. [PubMed][CrossRef]
123. Kim J, Hegde M, Kim SH, Wood TK, Jayaraman A. 2012. A microfluidic device for high throughput bacterial biofilm studies. Lab Chip 12:1157–1163. [PubMed][CrossRef]
124. Skolimowski M, Nielsen MW, Emnéus J, Molin S, Taboryski R, Sternberg C, Dufva M, Geschke O. 2010. Microfluidic dissolved oxygen gradient generator biochip as a useful tool in bacterial biofilm studies. Lab Chip 10:2162–2169. [PubMed][CrossRef]
125. Lee J-H, Kaplan J, Lee W. 2008. Microfluidic devices for studying growth and detachment of Staphylococcus epidermidis biofilms. Biomed Microdevices 10:489–498. [PubMed][CrossRef]
126. Rusconi R, Lecuyer S, Guglielmini L, Stone HA. 2010. Laminar flow around corners triggers the formation of biofilm streamers. J R Soc Interface 7:1293–1299. [PubMed][CrossRef]
127. Drescher K, Shen Y, Bassler BL, Stone HA. 2013. Biofilm streamers cause catastrophic disruption of flow with consequences for environmental and medical systems. Proc Natl Acad Sci USA 110:4345–4350. [PubMed][CrossRef]
128. Seminara A, Angelini TE, Wilking JN, Vlamakis H, Ebrahim S, Kolter R, Weitz DA, Brenner MP. 2011. Osmotic spreading of Bacillus subtilis biofilms driven by an extracellular matrix. Proc Natl Acad Sci USA 109:1116–1121. [PubMed][CrossRef]
129. Wilking JN, Angelini TE, Seminara A, Brenner MP, Weitz DA. 2011. Biofilms as complex fluids. MRS Bull 36:385–391. [CrossRef]
130. Hohne DN, Younger JG, Solomon MJ. 2009. Flexible microfluidic device for mechanical property characterization of soft viscoelastic solids such as bacterial biofilms. Langmuir 25:7743–7751. [PubMed][CrossRef]
131. De La Fuente L, Montanes E, Meng Y, Li Y, Burr TJ, Hoch H, Wu M. 2007. Assessing adhesion forces of type I and type IV pili of Xylella fastidiosa bacteria by use of a microfluidic flow chamber. Appl Environ Microbiol 73:2690–2696. [PubMed][CrossRef]
132. Nadell CD, Bassler BL. 2011. A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc Natl Acad Sci USA 108:14181–14185. [PubMed][CrossRef]
133. Hong SH, Hegde M, Kim J, Wang X, Jayaraman A, Wood TK. 2012. Synthetic quorum-sensing circuit to control consortial biofilm formation and dispersal in a microfluidic device. Nat Commun 3:613. [PubMed][CrossRef]
134. Metzker ML. 2010. Sequencing technologies: the next generation. Nat Rev Genet 11:31–46. [PubMed][CrossRef]
135. Flusberg BA, Webster DR, Lee JH, Travers KJ, Olivares EC, Clark TA, Korlach J, Turner SW. 2010. Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat Methods 7:461–465. [PubMed][CrossRef]
136. Goddard AF, Staudinger BJ, Dowd SE, Joshi-Datar A, Wolcott RD, Aitken ML, Fligner CL, Singh PK. 2012. Direct sampling of cystic fibrosis lungs indicates that DNA-based analyses of upper-airway specimens can misrepresent lung microbiota. Proc Natl Acad Sci USA 109:13769–13774. [PubMed][CrossRef]
137. Chivian D, Brodie EL, Alm EJ, Culley DE, Dehal PS, DeSantis TZ, Gihring TM, Lapidus A, Lin LH, Lowry SR, Moser DP, Richardson PM, Southam G, Wanger G, Pratt LM, Andersen GL, Hazen TC, Brockman FJ, Arkin AP, Onstott TC. 2008. Environmental genomics reveals a single-species ecosystem deep within Earth. Science 322:275–278. [PubMed][CrossRef]
138. Dick GJ, Andersson AF, Baker BJ, Simmons SL, Thomas BC, Yelton AP, Banfield JF. 2009. Community-wide analysis of microbial genome sequence signatures. Genome Biol 10:R85. [PubMed][CrossRef]
139. Goltsman DS, Dasari M, Thomas BC, Shah MB, VerBerkmoes NC, Hettich RL, Banfield JF. 2013. New group in the Leptospirillum clade: cultivation-independent community genomics, proteomics, and transcriptomics of the new species “ Leptospirillum group IV UBA BS.” Appl Environ Microbiol 79:5384–5393. [PubMed][CrossRef]
140. Yelton AP, Comolli LR, Justice NB, Castelle C, Denef VJ, Thomas BC, Banfield JF. 2013. Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea. BMC Genomics 14:485. [PubMed][CrossRef]
141. Inskeep WP, Jay ZJ, Herrgard MJ, Kozubal MA, Rusch DB, Tringe SG, Macur RE, Jennings R, Boyd ES, Spear JR, Roberto FF. 2013. Phylogenetic and functional analysis of metagenome sequence from high-temperature archaeal habitats demonstrate linkages between metabolic potential and geochemistry. Front Microbiol 4:95. [PubMed][CrossRef]
142. Klatt CG, Wood JM, Rusch DB, Bateson MM, Hamamura N, Heidelberg JF, Grossman AR, Bhaya D, Cohan FM, Kuhl M, Bryant DA, Ward DM. 2011. Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential. ISME J 5:1262–1278. [PubMed][CrossRef]
143. Klatt CG, Inskeep WP, Herrgard MJ, Jay ZJ, Rusch DB, Tringe SG, Niki Parenteau M, Ward DM, Boomer SM, Bryant DA, Miller SR. 2013. Community structure and function of high-temperature chlorophototrophic microbial mats inhabiting diverse geothermal environments. Front Microbiol 4:106. [PubMed][CrossRef]
144. Hasan NA, Young BA, Minard-Smith AT, Saeed K, Li H, Heizer EM, McMillan NJ, Isom R, Abdullah AS, Bornman DM, Faith SA, Choi SY, Dickens ML, Cebula TA, Colwell RR. 2014. Microbial community profiling of human saliva using shotgun metagenomic sequencing. PLoS One 9:e97699. doi:10.1371/journal.pone.0097699. [PubMed][CrossRef]
145. Wang J, Qi J, Zhao H, He S, Zhang Y, Wei S, Zhao F. 2013. Metagenomic sequencing reveals microbiota and its functional potential associated with periodontal disease. Sci Rep 3:1843. [PubMed][CrossRef]
146. Lozupone CA, Stombaugh J, Gonzalez A, Ackermann G, Wendel D, Vazquez-Baeza Y, Jansson JK, Gordon JI, Knight R. 2013. Meta-analyses of studies of the human microbiota. Genome Res 23:1704–1714. [PubMed][CrossRef]
147. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. 2007. The human microbiome project. Nature 449:804–810. [PubMed][CrossRef]
148. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI. 2009. A core gut microbiome in obese and lean twins. Nature 457:480–484. [PubMed][CrossRef]
149. Fullwood MJ, Wei CL, Liu ET, Ruan Y. 2009. Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses. Genome Res 19:521–532. [PubMed][CrossRef]
150. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. [PubMed][CrossRef]
151. Huson DH, Auch AF, Qi J, Schuster SC. 2007. MEGAN analysis of metagenomic data. Genome Res 17:377–386. [PubMed][CrossRef]
152. Huson DH, Richter DC, Mitra S, Auch AF, Schuster SC. 2009. Methods for comparative metagenomics. BMC Bioinformatics 10(Suppl 1) :S12. [PubMed][CrossRef]
153. Namiki T, Hachiya T, Tanaka H, Sakakibara Y. 2012. MetaVelvet: an extension of Velvet assembler to de novo metagenome assembly from short sequence reads. Nucleic Acids Res 40:e155. [PubMed][CrossRef]
154. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829. [PubMed][CrossRef]
155. McLean RJ, Kakirde KS. 2013. Enhancing metagenomics investigations of microbial interactions with biofilm technology. Int J Mol Sci 14:22246–22257. [PubMed][CrossRef]
156. Blainey PC. 2013. The future is now: single-cell genomics of bacteria and archaea. FEMS Microbiol Rev 37:407–427. [PubMed][CrossRef]
157. Landry ZC, Giovanonni SJ, Quake SR, Blainey PC. 2013. Optofluidic cell selection from complex microbial communities for single-genome analysis. Methods Enzymol 531:61–90. [PubMed][CrossRef]
158. McLean JS, Lombardo MJ, Badger JH, Edlund A, Novotny M, Yee-Greenbaum J, Vyahhi N, Hall AP, Yang Y, Dupont CL, Ziegler MG, Chitsaz H, Allen AE, Yooseph S, Tesler G, Pevzner PA, Friedman RM, Nealson KH, Venter JC, Lasken RS. 2013. Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum. Proc Natl Acad Sci USA 110:E2390–E2399. [PubMed][CrossRef]
159. Dean FB, Hosono S, Fang L, Wu X, Faruqi AF, Bray-Ward P, Sun Z, Zong Q, Du Y, Du J, Driscoll M, Song W, Kingsmore SF, Egholm M, Lasken RS. 2002. Comprehensive human genome amplification using multiple displacement amplification. Proc Natl Acad Sci USA 99:5261–5266. [PubMed][CrossRef]
160. Hentzer M, Eberl L, Givskov M. 2005. Transcriptome analysis of Pseudomonas aeruginosa biofilm development: anaerobic respiration and iron limitation. Biofilms 2:37–62. [CrossRef]
161. Mikkelsen H, Duck Z, Lilley KS, Welch M. 2007. Interrelationships between colonies, biofilms, and planktonic cells of Pseudomonas aeruginosa. J Bacteriol 189:2411–2416. [PubMed][CrossRef]
162. Schoolnik GK, Voskuil MI, Schnappinger D, Yildiz FH, Meibom K, Dolganov NA, Wilson MA, Chong KH. 2001. Whole genome DNA microarray expression analysis of biofilm development by Vibrio cholerae O1 E1 Tor. Methods Enzymol 336:3–18. [PubMed][CrossRef]
163. Waite RD, Paccanaro A, Papakonstantinopoulou A, Hurst JM, Saqi M, Littler E, Curtis MA. 2006. Clustering of Pseudomonas aeruginosa transcriptomes from planktonic cultures, developing and mature biofilms reveals distinct expression profiles. BMC Genomics 7:162. [PubMed][CrossRef]
164. Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teitzel GM, Lory S, Greenberg EP. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860–864. [PubMed][CrossRef]
165. Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Holko M, Yefanov A, Lee H, Zhang N, Robertson CL, Serova N, Davis S, Soboleva A. 2013. NCBI GEO: archive for functional genomics data sets: update. Nucleic Acids Res 41:D991–D995. [PubMed][CrossRef]
166. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207–210. [PubMed][CrossRef]
167. Stead MB, Marshburn S, Mohanty BK, Mitra J, Pena Castillo L, Ray D, van Bakel H, Hughes TR, Kushner SR. 2011. Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays. Nucleic Acids Res 39:3188–3203. [PubMed][CrossRef]
168. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, Balestrino D, Loh E, Gripenland J, Tiensuu T, Vaitkevicius K, Barthelemy M, Vergassola M, Nahori MA, Soubigou G, Regnault B, Coppee JY, Lecuit M, Johansson J, Cossart P. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950–956. [PubMed][CrossRef]
169. Wang Z, Gerstein M, Snyder M. 2009. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63. [PubMed][CrossRef]
170. Gifford S, Satinsky B, Moran MA. 2014. Quantitative microbial metatranscriptomics. Methods Mol Biol 1096:213–229. [PubMed][CrossRef]
171. Moran MA, Satinsky B, Gifford SM, Luo H, Rivers A, Chan LK, Meng J, Durham BP, Shen C, Varaljay VA, Smith CB, Yager PL, Hopkinson BM. 2013. Sizing up metatranscriptomics. ISME J 7:237–243. [PubMed][CrossRef]
172. Jorth P, Turner KH, Gumus P, Nizam N, Buduneli N, Whiteley M. 2014. Metatranscriptomics of the human oral microbiome during health and disease. MBio 5:e01012-01014. doi:10.1128/mBio.01012-14. [PubMed][CrossRef]
173. Klatt CG, Liu Z, Ludwig M, Kuhl M, Jensen SI, Bryant DA, Ward DM. 2013. Temporal metatranscriptomic patterning in phototrophic Chloroflexi inhabiting a microbial mat in a geothermal spring. ISME J 7:1775–1789. [PubMed][CrossRef]
174. Liu Z, Klatt CG, Wood JM, Rusch DB, Ludwig M, Wittekindt N, Tomsho LP, Schuster SC, Ward DM, Bryant DA. 2011. Metatranscriptomic analyses of chlorophototrophs of a hot-spring microbial mat. ISME J 5:1279–1290. [PubMed][CrossRef]
175. Cattoir V, Narasimhan G, Skurnik D, Aschard H, Roux D, Ramphal R, Jyot J, Lory S. 2013. Transcriptional response of mucoid Pseudomonas aeruginosa to human respiratory mucus. MBio 3:e00410-00412. doi:10.1128/mBio.00410-12. [PubMed][CrossRef]
176. Dugar G, Herbig A, Forstner KU, Heidrich N, Reinhardt R, Nieselt K, Sharma CM. 2013. High-resolution transcriptome maps reveal strain-specific regulatory features of multiple Campylobacter jejuni isolates. PLoS Genet 9:e1003495. doi:10.1371/journal.pgen.1003495. [PubMed][CrossRef]
177. Mandlik A, Livny J, Robins WP, Ritchie JM, Mekalanos JJ, Waldor MK. 2011. RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell Host Microbe 10:165–174. [PubMed][CrossRef]
178. Taveirne ME, Theriot CM, Livny J, DiRita VJ. 2013. The complete Campylobacter jejuni transcriptome during colonization of a natural host determined by RNAseq. PLoS One 8:e73586. doi:10.1371/journal.pone.0073586. [PubMed]
179. Pérez-Osorio AC, Williamson KS, Franklin MJ. 2010. Heterogeneous rpoS and rhlR mRNA levels and 16S rRNA/rDNA (rRNA gene) ratios within Pseudomonas aeruginosa biofilms, sampled by laser capture microdissection. J Bacteriol 192:2991–3000. [PubMed][CrossRef]
180. Van Oudenhove L, Devreese B. 2013. A review on recent developments in mass spectrometry instrumentation and quantitative tools advancing bacterial proteomics. Appl Microbiol Biotechnol 97:4749–4762. [PubMed][CrossRef]
181. Vaudel M, Sickmann A, Martens L. 2013. Introduction to opportunities and pitfalls in functional mass spectrometry based proteomics. Biochim Biophys Acta 1844:12–20. [PubMed][CrossRef]
182. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184:1140–1154. [PubMed][CrossRef]
183. Boes N, Schreiber K, Hartig E, Jaensch L, Schobert M. 2006. The Pseudomonas aeruginosa universal stress protein PA4352 is essential for surviving anaerobic energy stress. J Bacteriol 188:6529–6538. [PubMed][CrossRef]
184. Fong JC, Karplus K, Schoolnik GK, Yildiz FH. 2006. Identification and characterization of RbmA, a novel protein required for the development of rugose colony morphology and biofilm structure in Vibrio cholerae. J Bacteriol 188:1049–1059. [PubMed][CrossRef]
185. Kalmokoff M, Lanthier P, Tremblay TL, Foss M, Lau PC, Sanders G, Austin J, Kelly J, Szymanski CM. 2006. Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J Bacteriol 188:4312–4320. [PubMed][CrossRef]
186. Patrauchan MA, Sarkisova SA, Franklin MJ. 2007. Strain-specific proteome responses of Pseudomonas aeruginosa to biofilm-associated growth and to calcium. Microbiology 153:3838–3851. [PubMed][CrossRef]
187. Sarkisova S, Patrauchan MA, Berglund D, Nivens DE, Franklin MJ. 2005. Calcium-induced virulence factors associated with the extracellular matrix of mucoid Pseudomonas aeruginosa biofilms. J Bacteriol 187:4327–4337. [PubMed][CrossRef]
188. Rao J, Damron FH, Basler M, Digiandomenico A, Sherman NE, Fox JW, Mekalanos JJ, Goldberg JB. 2011. Comparisons of two proteomic analyses of non-mucoid and mucoid Pseudomonas aeruginosa clinical isolates from a cystic fibrosis patient. Front Microbiol 2:162. [PubMed][CrossRef]
189. Sauer K, Camper AK. 2001. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J Bacteriol 183:6579–6589. [PubMed][CrossRef]
190. Schreiber K, Boes N, Eschbach M, Jaensch L, Wehland J, Bjarnsholt T, Givskov M, Hentzer M, Schobert M. 2006. Anaerobic survival of Pseudomonas aeruginosa by pyruvate fermentation requires an Usp-type stress protein. J Bacteriol 188:659–668. [PubMed][CrossRef]
191. Wen ZT, Baker HV, Burne RA. 2006. Influence of BrpA on critical virulence attributes of Streptococcus mutans. J Bacteriol 188:2983–2992. [PubMed][CrossRef]
192. Unlu M, Morgan ME, Minden JS. 1997. Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18:2071–2077. [PubMed][CrossRef]
193. Tonge R, Shaw J, Middleton B, Rowlinson R, Rayner S, Young J, Pognan F, Hawkins E, Currie I, Davison M. 2001. Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics 1:377–396. [PubMed][CrossRef]
194. Marouga R, David S, Hawkins E. 2005. The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bioanal Chem 382:669–678. [PubMed][CrossRef]
195. Maaty WS, Wiedenheft B, Tarlykov P, Schaff N, Heinemann J, Robison-Cox J, Valenzuela J, Dougherty A, Blum P, Lawrence CM, Douglas T, Young MJ, Bothner B. 2009. Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress. PLoS One 4:e6964. doi:10.1371/journal.pone.0006964. [PubMed][CrossRef]
196. Petrova OE, Sauer K. 2012. Dispersion by Pseudomonas aeruginosa requires an unusual posttranslational modification of BdlA. Proc Natl Acad Sci USA 109:16690–16695. [PubMed][CrossRef]
197. Denef VJ, Shah MB, Verberkmoes NC, Hettich RL, Banfield JF. 2007. Implications of strain- and species-level sequence divergence for community and isolate shotgun proteomic analysis. J Proteome Res 6:3152–3161. [PubMed][CrossRef]
198. Jiao Y, D’Haeseleer P, Dill BD, Shah M, Verberkmoes NC, Hettich RL, Banfield JF, Thelen MP. 2011. Identification of biofilm matrix-associated proteins from an acid mine drainage microbial community. Appl Environ Microbiol 77:5230–5237. [PubMed][CrossRef]
199. Pessi G, Braunwalder R, Grunau A, Omasits U, Ahrens CH, Eberl L. 2013. Response of Burkholderia cenocepacia H111 to micro-oxia. PLoS One 8:e72939. doi:10.1371/journal.pone.0072939. [PubMed][CrossRef]
200. Santi L, Beys-da-Silva WO, Berger M, Calzolari D, Guimaraes JA, Moresco JJ, Yates JR, 3rd. 2014. Proteomic profile of Cryptococcus neoformans biofilm reveals changes in metabolic processes. J Proteome Res 13:1545–1559. [PubMed][CrossRef]
201. Schmid N, Pessi G, Deng Y, Aguilar C, Carlier AL, Grunau A, Omasits U, Zhang LH, Ahrens CH, Eberl L. 2012. The AHL- and BDSF-dependent quorum sensing systems control specific and overlapping sets of genes in Burkholderia cenocepacia H111. PLoS One 7:e49966. doi:10.1371/journal.pone.0049966. [PubMed][CrossRef]
202. Wu WL, Liao JH, Lin GH, Lin MH, Chang YC, Liang SY, Yang FL, Khoo KH, Wu SH. 2013. Phosphoproteomic analysis reveals the effects of PilF phosphorylation on type IV pilus and biofilm formation in Thermus thermophilus HB27. Mol Cell Proteomics 12:2701–2713. [PubMed][CrossRef]
203. Vera M, Krok B, Bellenberg S, Sand W, Poetsch A. 2013. Shotgun proteomics study of early biofilm formation process of Acidithiobacillus ferrooxidans ATCC 23270 on pyrite. Proteomics 13:1133–1144. [PubMed][CrossRef]
204. Wolters DA, Washburn MP, Yates JR, 3rd. 2001. An automated multidimensional protein identification technology for shotgun proteomics. Anal Chem 73:5683–5690. [PubMed][CrossRef]
205. Cabral MP, Soares NC, Aranda J, Parreira JR, Rumbo C, Poza M, Valle J, Calamia V, Lasa I, Bou G. 2011. Proteomic and functional analyses reveal a unique lifestyle for Acinetobacter baumannii biofilms and a key role for histidine metabolism. J Proteome Res 10:3399–3417. [PubMed][CrossRef]
206. Chopra S, Ramkissoon K, Anderson DC. 2013. A systematic quantitative proteomic examination of multidrug resistance in Acinetobacter baumannii. J Proteomics 84:17–39. [PubMed][CrossRef]
207. Evans C, Noirel J, Ow SY, Salim M, Pereira-Medrano AG, Couto N, Pandhal J, Smith D, Pham TK, Karunakaran E, Zou X, Biggs CA, Wright PC. 2012. An insight into iTRAQ: where do we stand now? Anal Bioanal Chem 404:1011–1027. [PubMed][CrossRef]
208. Huynh TT, McDougald D, Klebensberger J, Al Qarni B, Barraud N, Rice SA, Kjelleberg S, Schleheck D. 2012. Glucose starvation-induced dispersal of Pseudomonas aeruginosa biofilms is cAMP and energy dependent. PLoS One 7:e42874. doi:10.1371/journal.pone.0042874. [PubMed][CrossRef]
209. Pham TK, Roy S, Noirel J, Douglas I, Wright PC, Stafford GP. 2010. A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia. Proteomics 10:3130–3141. [PubMed][CrossRef]
210. Solis N, Parker BL, Kwong SM, Robinson G, Firth N, Cordwell SJ. 2014. Staphylococcus aureus surface proteins involved in adaptation to oxacillin identified using a novel cell shaving approach. J Proteome Res 13:2954–2972. [PubMed][CrossRef]
211. Booth SC, Workentine ML, Wen J, Shaykhutdinov R, Vogel HJ, Ceri H, Turner RJ, Weljie AM. 2011. Differences in metabolism between the biofilm and planktonic response to metal stress. J Proteome Res 10:3190–3199. [PubMed][CrossRef]
212. Kouremenos KA, Beale DJ, Antti H, Palombo EA. 2014. Liquid chromatography time of flight mass spectrometry based environmental metabolomics for the analysis of Pseudomonas putida bacteria in potable water. J Chromatogr B Analyt Technol Biomed Life Sci 966:179–86. [PubMed][CrossRef]
213. Martinez P, Galvez S, Ohtsuka N, Budinich M, Cortes MP, Serpell C, Nakahigashi K, Hirayama A, Tomita M, Soga T, Martinez S, Maass A, Parada P. 2013. Metabolomic study of Chilean biomining bacteria Acidithiobacillus ferrooxidans strain Wenelen and Acidithiobacillus thiooxidans strain Licanantay. Metabolomics 9:247–257. [PubMed][CrossRef]
214. Mosier AC, Justice NB, Bowen BP, Baran R, Thomas BC, Northen TR, Banfield JF. 2013. Metabolites associated with adaptation of microorganisms to an acidophilic, metal-rich environment identified by stable-isotope-enabled metabolomics. MBio 4:e00484-00412. doi:10.1128/mBio.00484-12.
215. White AP, Weljie AM, Apel D, Zhang P, Shaykhutdinov R, Vogel HJ, Surette MG. 2010. A global metabolic shift is linked to Salmonella multicellular development. PLoS One 5:e11814. doi:10.1371/journal.pone.0011814. [PubMed][CrossRef]
216. Workentine ML, Harrison JJ, Weljie AM, Tran VA, Stenroos PU, Tremaroli V, Vogel HJ, Ceri H, Turner RJ. 2010. Phenotypic and metabolic profiling of colony morphology variants evolved from Pseudomonas fluorescens biofilms. Environ Microbiol 12:1565–1577. [PubMed]
217. Want EJ, O’Maille G, Smith CA, Brandon TR, Uritboonthai W, Qin C, Trauger SA, Siuzdak G. 2006. Solvent-dependent metabolite distribution, clustering, and protein extraction for serum profiling with mass spectrometry. Anal Chem 78:743–752. [PubMed][CrossRef]
218. Want EJ, Cravatt BF, Siuzdak G. 2005. The expanding role of mass spectrometry in metabolite profiling and characterization. Chembiochem 6:1941–1951. [PubMed][CrossRef]
219. Tautenhahn R, Patti GJ, Kalisiak E, Miyamoto T, Schmidt M, Lo FY, McBee J, Baliga NS, Siuzdak G. 2010. metaXCMS: second-order analysis of untargeted metabolomics data. Anal Chem 83:696–700. [PubMed][CrossRef]
220. Smith CA, O’Maille G, Want EJ, Qin C, Trauger SA, Brandon TR, Custodio DE, Abagyan R, Siuzdak G. 2005. METLIN: a metabolite mass spectral database. Ther Drug Monit 27:747–751. [PubMed][CrossRef]
221. Tautenhahn R, Cho K, Uritboonthai W, Zhu Z, Patti GJ, Siuzdak G. 2012. An accelerated workflow for untargeted metabolomics using the METLIN database. Nat Biotechnol 30:826–828. [PubMed][CrossRef]
222. Wishart DS, Knox C, Guo AC, Eisner R, Young N, Gautam B, Hau DD, Psychogios N, Dong E, Bouatra S, Mandal R, Sinelnikov I, Xia J, Jia L, Cruz JA, Lim E, Sobsey CA, Shrivastava S, Huang P, Liu P, Fang L, Peng J, Fradette R, Cheng D, Tzur D, Clements M, Lewis A, De Souza A, Zuniga A, Dawe M, Xiong Y, Clive D, Greiner R, Nazyrova A, Shaykhutdinov R, Li L, Vogel HJ, Forsythe I. 2009. HMDB: a knowledgebase for the human metabolome. Nucleic Acids Res 37:D603–D610. [PubMed][CrossRef]
223. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642–1645. [PubMed][CrossRef]
224. Hess ST, Girirajan TP, Mason MD. 2006. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91:4258–4272. [PubMed][CrossRef]
225. Rust MJ, Bates M, Zhuang X. 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3:793–795. [PubMed][CrossRef]
226. Neu TR, Lawrence JR. 2014. Investigation of microbial biofilm structure by laser scanning microscopy. Adv Biochem Eng Biotechnol 146:1–51. [PubMed][CrossRef]
227. Jackson KD, Starkey M, Kremer S, Parsek MR, Wozniak DJ. 2004. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186:4466–4475. [PubMed][CrossRef]
228. Barken KB, Pamp SJ, Yang L, Gjermansen M, Bertrand JJ, Klausen M, Givskov M, Whitchurch CB, Engel JN, Tolker-Nielsen T. 2008. Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ Microbiol 10:2331–2343. [PubMed][CrossRef]
229. Christen B, Fero MJ, Hillson NJ, Bowman G, Hong SH, Shapiro L, McAdams HH. 2010. High-throughput identification of protein localization dependency networks. Proc Natl Acad Sci USA 107:4681–4686. [PubMed][CrossRef]
230. Lew MD, Lee SF, Ptacin JL, Lee MK, Twieg RJ, Shapiro L, Moerner WE. 2011. Three-dimensional superresolution colocalization of intracellular protein superstructures and the cell surface in live Caulobacter crescentus. Proc Natl Acad Sci USA 108:E1102–E1110. [PubMed][CrossRef]
231. Li G, Young KD. 2012. Isolation and identification of new inner membrane-associated proteins that localize to cell poles in Escherichia coli. Mol Microbiol 84:276–295. [PubMed][CrossRef]
232. Lindner AB, Madden R, Demarez A, Stewart EJ, Taddei F. 2008. Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc Natl Acad Sci USA 105:3076–3081. [PubMed][CrossRef]
233. Chai Y, Chu F, Kolter R, Losick R. 2008. Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 67:254–263. [PubMed][CrossRef]
234. Lydmark P, Lind M, Sørensson F, Hermansson M. 2006. Vertical distribution of nitrifying populations in bacterial biofilms from a full-scale nitrifying trickling filter. Environ Microbiol 8:2036–2049. [PubMed][CrossRef]
235. Kofoed MV, Nielsen DA, Revsbech NP, Schramm A. 2012. Fluorescence in situ hybridization (FISH) detection of nitrite reductase transcripts (nirS mRNA) in Pseudomonas stutzeri biofilms relative to a microscale oxygen gradient. Syst Appl Microbiol 35:513–517. [PubMed][CrossRef]
236. Rosenthal AZ, Zhang X, Lucey KS, Ottesen EA, Trivedi V, Choi HM, Pierce NA, Leadbetter JR. 2013. Localizing transcripts to single cells suggests an important role of uncultured deltaproteobacteria in the termite gut hydrogen economy. Proc Natl Acad Sci USA 110:16163–16168. [PubMed][CrossRef]
237. Behnam F, Vilcinskas A, Wagner M, Stoecker K. 2012. A straightforward DOPE (double labeling of oligonucleotide probes)-FISH (fluorescence in situ hybridization) method for simultaneous multicolor detection of six microbial populations. Appl Environ Microbiol 78:5138–5142. [PubMed][CrossRef]
238. Valm AM, Mark Welch JL, Rieken CW, Hasegawa Y, Sogin ML, Oldenbourg R, Dewhirst FE, Borisy GG. 2011. Systems-level analysis of microbial community organization through combinatorial labeling and spectral imaging. Proc Natl Acad Sci USA 108:4152–4157. [PubMed][CrossRef]
239. Valm AM, Mark Welch JL, Borisy GG. 2012. CLASI-FISH: principles of combinatorial labeling and spectral imaging. Syst Appl Microbiol 35:496–502. [PubMed][CrossRef]
240. Schneider D, Fuhrmann E, Scholz I, Hess WR, Graumann PL. 2007. Fluorescence staining of live cyanobacterial cells suggest non-stringent chromosome segregation and absence of a connection between cytoplasmic and thylakoid membranes. BMC Cell Biol 8:39. [PubMed][CrossRef]
241. Créach V, Baudoux AC, Bertru G, Rouzic BL. 2003. Direct estimate of active bacteria: CTC use and limitations. J Microbiol Methods 52:19–28. [PubMed][CrossRef]
242. Nielsen JL, Aquino de Muro M, Nielsen PH. 2003. Evaluation of the redox dye 5-cyano-2,3-tolyl-tetrazolium chloride for activity studies by simultaneous use of microautoradiography and fluorescence in situ hybridization. Appl Environ Microbiol 69:641–643. [PubMed][CrossRef]
243. Breinbauer R, Kohn M. 2003. Azide-alkyne coupling: a powerful reaction for bioconjugate chemistry. Chembiochem 4:1147–1149. [PubMed][CrossRef]
244. Liechti GW, Kuru E, Hall E, Kalinda A, Brun YV, VanNieuwenhze M, Maurelli AT. 2014. A new metabolic cell-wall labelling method reveals peptidoglycan in Chlamydia trachomatis. Nature 506:507–510. [PubMed][CrossRef]
245. Siegrist MS, Whiteside S, Jewett JC, Aditham A, Cava F, Bertozzi CR. 2013. (D)-amino acid chemical reporters reveal peptidoglycan dynamics of an intracellular pathogen. ACS Chem Biol 8:500–505. [PubMed][CrossRef]
246. Spiers AJ, Bohannon J, Gehrig SM, Rainey PB. 2003. Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 50:15–27. [PubMed][CrossRef]
247. Elzinga EJ, Huang JH, Chorover J, Kretzschmar R. 2012. ATR-FTIR spectroscopy study of the influence of pH and contact time on the adhesion of Shewanella putrefaciens bacterial cells to the surface of hematite. Environ Sci Technol 46:12848–12855. [PubMed][CrossRef]
248. Quilès F, Humbert F. 2014. On the production of glycogen by Pseudomonas fluorescens during biofilm development: an in situ study by attenuated total reflection-infrared with chemometrics. Biofouling 30:709–718. [PubMed][CrossRef]
249. Suci PA, Geesey GG, Tyler BJ. 2001. Integration of Raman microscopy, differential interference contrast microscopy, and attenuated total reflection Fourier transform infrared spectroscopy to investigate chlorhexidine spatial and temporal distribution in Candida albicans biofilms. J Microbiol Methods 46:193–208. [PubMed][CrossRef]
250. Holman HY, Miles R, Hao Z, Wozei E, Anderson LM, Yang H. 2009. Real-time chemical imaging of bacterial activity in biofilms using open-channel microfluidics and synchrotron FTIR spectromicroscopy. Anal Chem 81:8564–8570. [PubMed][CrossRef]
251. Pätzold R, Keuntje M, Theophile K, Muller J, Mielcarek E, Ngezahayo A, Anders-von Ahlften A. 2008. In situ mapping of nitrifiers and anammox bacteria in microbial aggregates by means of confocal resonance Raman microscopy. J Microbiol Methods 72:241–248. [PubMed][CrossRef]
252. Pätzold R, Keuntje M, Anders-von Ahlften A. 2006. A new approach to non-destructive analysis of biofilms by confocal Raman microscopy. Anal Bioanal Chem 386:286–292. [PubMed][CrossRef]
253. Sandt C, Smith-Palmer T, Pink J, Brennan L, Pink D. 2007. Confocal Raman microspectroscopy as a tool for studying the chemical heterogeneities of biofilms in situ. J Appl Microbiol 103:1808–1820. [PubMed][CrossRef]
254. Sandt C, Smith-Palmer T, Comeau J, Pink D. 2009. Quantification of water and biomass in small colony variant PAO1 biofilms by confocal Raman microspectroscopy. Appl Microbiol Biotechnol 83:1171–1182. [PubMed][CrossRef]
255. Chao Y, Zhang T. 2012. Surface-enhanced Raman scattering (SERS) revealing chemical variation during biofilm formation: from initial attachment to mature biofilm. Anal Bioanal Chem 404:1465–1475. [PubMed][CrossRef]
256. Ivleva NP, Wagner M, Horn H, Niessner R, Haisch C. 2008. In situ surface-enhanced Raman scattering analysis of biofilm. Anal Chem 80:8538–8544. [PubMed][CrossRef]
257. Ivleva NP, Wagner M, Szkola A, Horn H, Niessner R, Haisch C. 2010. Label-free in situ SERS imaging of biofilms. J Phys Chem B 114:10184–10194. [PubMed][CrossRef]
258. Wagner M, Ivleva NP, Haisch C, Niessner R, Horn H. 2009. Combined use of confocal laser scanning microscopy (CLSM) and Raman microscopy (RM): investigations on EPS-matrix. Water Res 43:63–76. [PubMed][CrossRef]
259. Chang CB, Wilking JN, Kim S-H, Shum HC, Weitz DA. 2015. Monodisperse emulsion drop microenvironments for bacterial biofilm growth. Small doi:10.1002/smll.201403125. [PubMed][CrossRef]
260. Alonso C. 2012. Tips and tricks for high quality MAR-FISH preparations: focus on bacterioplankton analysis. Syst Appl Microbiol 35:503–512. [PubMed][CrossRef]
261. Tischer K, Zeder M, Klug R, Pernthaler J, Schattenhofer M, Harms H, Wendeberg A. 2012. Fluorescence in situ hybridization (CARD-FISH) of microorganisms in hydrocarbon contaminated aquifer sediment samples. Syst Appl Microbiol 35:526–532. [PubMed][CrossRef]
262. Majors PD, McLean JS, Pinchuk GE, Fredrickson JK, Gorby YA, Minard KR, Wind RA. 2005. NMR methods for in situ biofilm metabolism studies. J Microbiol Methods 62:337–344. [PubMed][CrossRef]
263. Renslow RS, Majors PD, McLean JS, Fredrickson JK, Ahmed B, Beyenal H. 2010. In situ effective diffusion coefficient profiles in live biofilms using pulsed-field gradient nuclear magnetic resonance. Biotechnol Bioeng 106:928–937. [PubMed][CrossRef]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.MB-0016-2014
2015-08-21
2021-04-13

Abstract:

Bacteria have traditionally been studied as single-cell organisms. In laboratory settings, aerobic bacteria are usually cultured in aerated flasks, where the cells are considered essentially homogenous. However, in many natural environments, bacteria and other microorganisms grow in mixed communities, often associated with surfaces. Biofilms are comprised of surface-associated microorganisms, their extracellular matrix material, and environmental chemicals that have adsorbed to the bacteria or their matrix material. While this definition of a biofilm is fairly simple, biofilms are complex and dynamic. Our understanding of the activities of individual biofilm cells and whole biofilm systems has developed rapidly, due in part to advances in molecular, analytical, and imaging tools and the miniaturization of tools designed to characterize biofilms at the enzyme level, cellular level, and systems level.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/3/4/MB-0016-2014.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.MB-0016-2014&mimeType=html&fmt=ahah

Figures

New Technologies for Studying Biofilms
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-1,properties={foaf_givenname=Michael J., foaf_name=Michael J. Franklin, foaf_surname=Franklin, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MB-0016-2014-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-2,properties={foaf_givenname=Connie, foaf_name=Connie Chang, foaf_surname=Chang, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MB-0016-2014-aff3]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-3,webId=/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-3,properties={foaf_givenname=Tatsuya, foaf_name=Tatsuya Akiyama, foaf_surname=Akiyama, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MB-0016-2014-aff5]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-4,webId=/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-4,properties={foaf_givenname=Brian, foaf_name=Brian Bothner, foaf_surname=Bothner, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MB-0016-2014-aff7]]}]]
Citation: Franklin M, Chang C, Akiyama T, Bothner B. 2015. New technologies for studying biofilms. microbiolspec 3(4): doi:10.1128/microbiolspec.MB-0016-2014
/content/microbiolspec/10.1128/microbiolspec.MB-0016-2014.fig1
FIGURE 1
Examples of methods for biofilm cultivation under static conditions. (A) Biofilm cultured at the air-water interface, forming a pellicle. Published with permission from reference 83 . (B) Biofilm cultured on a glass coupon under static conditions. Published with permission from reference 84 . (C) Example of biofilm growth as a colony biofilm. Published with permission from reference 84 .
microbiolspec/3/4/MB-0016-2014-fig1_thmb.gif
microbiolspec/3/4/MB-0016-2014-fig1.gif
Image of FIGURE 1

Click to view

FIGURE 1

Examples of methods for biofilm cultivation under static conditions. (A) Biofilm cultured at the air-water interface, forming a pellicle. Published with permission from reference 83 . (B) Biofilm cultured on a glass coupon under static conditions. Published with permission from reference 84 . (C) Example of biofilm growth as a colony biofilm. Published with permission from reference 84 .

Source: microbiolspec August 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0016-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MB-0016-2014.fig2
FIGURE 2
Examples of continuous-flow reactors for biofilm cultivation. (A) CDC reactor with medium inlet and outlet ports. Biofilms form on coupons arranged on removable Teflon rods. Published with permission from reference 88 . (B) Drip-flow reactor with medium inlet and outlet ports and air exchange ports. Biofilms form on removable slides. Published with permission from reference 89 . (C) Capillary flow cell for imaging biofilms. Published with permission from http://centerforgenomicsciences.org/research/biofilm_flow.html.
microbiolspec/3/4/MB-0016-2014-fig2_thmb.gif
microbiolspec/3/4/MB-0016-2014-fig2.gif
Image of FIGURE 2

Click to view

FIGURE 2

Examples of continuous-flow reactors for biofilm cultivation. (A) CDC reactor with medium inlet and outlet ports. Biofilms form on coupons arranged on removable Teflon rods. Published with permission from reference 88 . (B) Drip-flow reactor with medium inlet and outlet ports and air exchange ports. Biofilms form on removable slides. Published with permission from reference 89 . (C) Capillary flow cell for imaging biofilms. Published with permission from http://centerforgenomicsciences.org/research/biofilm_flow.html.

Source: microbiolspec August 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0016-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MB-0016-2014.fig3
FIGURE 3
Examples of microfluidics approaches applied to biofilm research. (A) Example of a microfluidics device for precise control of fluids. Published with permission from reference 110 . (B) Biofilm streamers forming within a microfluidics flow channel. Published with permission from reference 127 . Microdroplet biofilm reactor showing phenotypic switching of cells and simultaneous change in expression from cyan fluorescent protein to the yellow fluorescent protein Published with permission from reference 259 . (D) Schematic representation of microfluidics flow cell. Published with permission from reference 133 .
microbiolspec/3/4/MB-0016-2014-fig3_thmb.gif
microbiolspec/3/4/MB-0016-2014-fig3.gif
Image of FIGURE 3

Click to view

FIGURE 3

Examples of microfluidics approaches applied to biofilm research. (A) Example of a microfluidics device for precise control of fluids. Published with permission from reference 110 . (B) Biofilm streamers forming within a microfluidics flow channel. Published with permission from reference 127 . Microdroplet biofilm reactor showing phenotypic switching of cells and simultaneous change in expression from cyan fluorescent protein to the yellow fluorescent protein Published with permission from reference 259 . (D) Schematic representation of microfluidics flow cell. Published with permission from reference 133 .

Source: microbiolspec August 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0016-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MB-0016-2014.fig4
FIGURE 4
Example of a biofilm vertical transect, showing GFP–gene expression heterogeneity. Areas were cut from different biofilm strata and captured for transcriptomics analyses. Published with permission from reference 61 .
microbiolspec/3/4/MB-0016-2014-fig4_thmb.gif
microbiolspec/3/4/MB-0016-2014-fig4.gif
Image of FIGURE 4

Click to view

FIGURE 4

Example of a biofilm vertical transect, showing GFP–gene expression heterogeneity. Areas were cut from different biofilm strata and captured for transcriptomics analyses. Published with permission from reference 61 .

Source: microbiolspec August 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0016-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MB-0016-2014.fig5
FIGURE 5
Gene expression heterogeneity, demonstrated by translational fusions of target proteins to the yellow fluorescent protein (YFP). (A) Translational fusion of the IbpA protein to YFP, showing uniform distribution of IbpA throughout the biofilm. Cells were counterstained with mCherry fluorescent protein (mCFP). (B) Translational fusion of Rmf protein to YFP, showing that most Rmf production occurs in cells at the top of the biofilm. Cells counterstained with mCFP (M.J. Franklin, unpublished data).
microbiolspec/3/4/MB-0016-2014-fig5_thmb.gif
microbiolspec/3/4/MB-0016-2014-fig5.gif
Image of FIGURE 5

Click to view

FIGURE 5

Gene expression heterogeneity, demonstrated by translational fusions of target proteins to the yellow fluorescent protein (YFP). (A) Translational fusion of the IbpA protein to YFP, showing uniform distribution of IbpA throughout the biofilm. Cells were counterstained with mCherry fluorescent protein (mCFP). (B) Translational fusion of Rmf protein to YFP, showing that most Rmf production occurs in cells at the top of the biofilm. Cells counterstained with mCFP (M.J. Franklin, unpublished data).

Source: microbiolspec August 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0016-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MB-0016-2014.fig6
FIGURE 6
(A) Images of biofilms, where the cells constitutively express the GFP. (B) Extracellular matrix material stained with Bodipy 630/650-X NHS from Life Technologies. (C) Combined image showing GFP-fluorescent bacteria and Bodipy-stained matrix (M.J. Franklin, unpublished data).
microbiolspec/3/4/MB-0016-2014-fig6_thmb.gif
microbiolspec/3/4/MB-0016-2014-fig6.gif
Image of FIGURE 6

Click to view

FIGURE 6

(A) Images of biofilms, where the cells constitutively express the GFP. (B) Extracellular matrix material stained with Bodipy 630/650-X NHS from Life Technologies. (C) Combined image showing GFP-fluorescent bacteria and Bodipy-stained matrix (M.J. Franklin, unpublished data).

Source: microbiolspec August 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0016-2014
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

New Technologies for Studying Biofilms
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-1,properties={foaf_givenname=Michael J., foaf_name=Michael J. Franklin, foaf_surname=Franklin, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MB-0016-2014-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-2,properties={foaf_givenname=Connie, foaf_name=Connie Chang, foaf_surname=Chang, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MB-0016-2014-aff3]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-3,webId=/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-3,properties={foaf_givenname=Tatsuya, foaf_name=Tatsuya Akiyama, foaf_surname=Akiyama, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MB-0016-2014-aff5]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-4,webId=/content/author/microbiolspec/10.1128/microbiolspec.MB-0016-2014-4,properties={foaf_givenname=Brian, foaf_name=Brian Bothner, foaf_surname=Bothner, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MB-0016-2014-aff7]]}]]
Citation: Franklin M, Chang C, Akiyama T, Bothner B. 2015. New technologies for studying biofilms. microbiolspec 3(4): doi:10.1128/microbiolspec.MB-0016-2014
/content/microbiolspec/10.1128/microbiolspec.MB-0016-2014.T1
TABLE 1
Methods for cultivation of biofilms
Generic image for table

Click to view

TABLE 1

Methods for cultivation of biofilms

Source: microbiolspec August 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0016-2014
/content/microbiolspec/10.1128/microbiolspec.MB-0016-2014.T2
TABLE 2
Imaging strategies in biofilm studies
Generic image for table

Click to view

TABLE 2

Imaging strategies in biofilm studies

Source: microbiolspec August 2015 vol. 3 no. 4 doi:10.1128/microbiolspec.MB-0016-2014

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error