Abstract
The ecology in a biofilm—i.e., how the cells relate to each other and their environment—can offer competitive advantages over an autonomous, free-swimming, planktonic environment such as nutrient acquisition via cross-feeding of populations and increased resistance to biocides. To explore this ecology, we investigated the physical parameters governing prokaryotic cell-to-cell signaling in a simple model of a biofilm created using live-cell lithography, comprising bacteria that are genetically engineered to transmit and receive quorum-sensing signals. These experiments, along with the numerical simulations that mirror them, revealed that gene expression resulting from transmitter to receiver communications was vitally dependent on the location within the biofilm elements and the epigenetic memory associated with a bistable switch in the receiver gene, which were both easily accessible in the model. Three-dimensional biofilm models with open channels that include still more complex communication networks for the study of wound repair are in the offing.
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References
Hall-Stoodley L, Costerton J, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95
Flemming H-C, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623
Costerton JW, Lappin-Scott HM (1989) Behavior of bacteria in biofilms. Am Soc Microbiol News 55:650
Chauret C, Volk C, Creason R, Jarosh L, Robinson J, Warnes C (2001) Detection of Aeromonas hydrophila in a drinking-water distribution system: a field and pilot study. Can J Microbiol 47:782
Stickler DJ (2008) Bacterial biofilms in patients with indwelling urinary catheters. Nat Clin Pract Urol 5:598
Ramage G, Martinez JP, Lopez-Ribot JL (2006) Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res 6:979
Lewis K (2001) Riddle of biofilm resistance. Antimicrob Agents Chemother 45:999
Kharazmi A, Giwercman B, Høiby N (1999) Robbins device in biofilm research. Methods Enzymol 310:207
Stoodley P, Dodds I, De Beer D, Scott H, Boyle J (2005) Flowing biofilms as a transport mechanism for biomass through porous media under laminar and turbulent conditions in a laboratory reactor system. Biofouling 21:161
Augspurger C, Karwautz C, Mussmann M, Daims H, Battin T (2010) Drivers of bacterial colonization patterns in stream biofilms. FEMS Microbiol Ecol 72:47
Dufour D, Leung V, LĂ©vesque CM (2012) Bacterial biofilm: structure, function, and antimicrobial resistance. Endo Topics 22:2
Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439
Hentzer M, Givskov M, Eberl L (2004) Microbial biofilms. In: Mahmoud G (ed) ASM, Washington, DC, p 118
Pappas KM, Weingart CL, Winans SC (2004) Chemical communication in proteobacteria: biochemical and structural studies of signal synthases and receptors required for intercellular signalling. Mol Microbiol 53:755
Shirtliff ME, Mader JT, Camper AK (2002) Molecular interactions in biofilms. Chem Biol 9:859
De Kievit TR, Iglewski BH (2000) Bacterial quorum sensing in pathogenic relationships. Infect Immun 68:4839
Timp W, Mirsaidov U, Matsudaira P, Timp G (2009) Jamming prokaryotic cell-to-cell communications in a model biofilm. Lab Chip 9:925
Redfield R (2002) Is quorum sensing a side effect of diffusion sensing? Trends Microbiol 10:365
Hense BA, Kuttler C, MĂĽller J, Rothballer M, Hartmann A, Kreft J-U (2007) Does efficiency sensing unify diffusion and quorum sensing? Nat Rev Microbiol 5:230
Horswill AR, Stoodley P, Stewart PS, Parsek MR (2007) The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities. Anal Bioanal Chem 387:371
Nelson EM, Kurz V, Perry N, Kyrouac D, Timp G (2014) Biological noise abatement: coordinating the responses of autonomous bacteria in a synthetic biofilm to a fluctuating environment using a stochastic bistable switch. ACS Synth Biol 3:286
Pedraza JM, van Oudenaarden A (2005) Noise propagation in gene networks. Science 307:1965
Raser JM, O’Shea EK (2005) Noise in gene expression: origins, consequences, and control. Science 309:2010
Samoilov MS, Price G, Arkin AP (2006) From fluctuations to phenotypes: the physiology of noise. Sci STKE 2006:re17
Thattai M, van Oudenaarden A (2004) Stochastic gene expression in fluctuating environments. Genetics 167:523
Mirsaidov U, Scrimgeour J, Timp W, Beck K, Mir M, Matsudaira P, Timp G (2008) Live cell lithography: using optical tweezers to create synthetic tissue. Lab Chip 8:2174
Kurz V, Nelson E, Perry N, Timp W, Timp G (2013) Epigenetic memory emerging from integrated transcription bursts. Biophys J 105:1526
Akselrod G, Timp W, Mirsaidov U, Zhao Q, Li C, Timp R, Timp K, Matsudaira P, Timp G (2006) Laser-guided assembly of heterotypic three-dimensional living cell microarrays. Biophys J 91:3465
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165
Bassler BL, Losick R (2006) Bacterially speaking. Cell 125:237
Goryachev AB, Toh DJ, Lee T (2006) Systems analysis of a quorum sensing network: design constraints imposed by the functional requirements, network topology and kinetic constants. Biosystems 83:178
Stamatakis M, Mantzaris NV (2009) Comparison of deterministic and stochastic models of the lac operon genetic network. Biophys J 96:887
Blake WJ, Balázsi G, Kohanski MA, Isaacs FJ, Murphy KF, Kuang Y, Cantor CR, Walt DR, Collins JJ (2006) Phenotypic consequences of promoter-mediated transcriptional noise. Mol Cell 24:853–865
Ozbudak EM, Thattai M, Kurtser I, Grossman AD, van Oudenaarden A (2002) Regulation of noise in the expression of a single gene. Nat Genet 31:69–73
McAdams HH, Arkin A (1997) Stochastic mechanisms in gene expression. Proc Natl Acad Sci U S A 94:814–819
Danino T, MondragĂłn-Palomino O, Tsimring L, Hasty J (2010) A synchronized quorum of genetic clocks. Nature 463:326
Rao CV, Wolf DM, Arkin AP (2002) Control, exploitation and tolerance of intracellular noise. Nature 420:231–237
Hui EE, Bhatia SN (2007) Micromechanical control of cell–cell interactions. Proc Natl Acad Sci U S A 104:5722
Chen C, Mrksich M, Huang S, Whitesides G, Ingber D (1997) Geometric control of cell life and death. Science 276:1425
Ozkan M, Pisanic T, Scheel J, Barlow C, Esener S, Bhatia SN (2003) Electrooptical platform for the manipulation of live cells. Langmuir 19:1532
Albrecht DR, Underhill GH, Wassermann TB, Sah RL, Bhatia SN (2006) Probing the role of multicellular organization in three-dimensional microenvironments. Nat Methods 3:369
Golden AP, Tien J (2007) Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip 7:720
Ling Y, Rubin J, Deng Y, Huang C, Demirici U, Karp JM, Khademhosseini A (2007) A cell-laden microfluidic hydrogel. Lab Chip 7:756
Visconti RP, Kasyanov V, Gentile C, Zhang J, Markwald RR, Mironov V (2010) Towards organ printing: engineering an intra-organ branched vascular tree. Expert Opin Biol Ther 10:409
Jakab K, Norotte C, Marga F, Murphy K, Vunjak-Novakovic G, Forgacs G (2010) Tissue engineering by self-assembly and bio-printing of living cells. Biofabrication 2:022001
Rezende RA, de Souza Azevedo F, Pereira FD, Kasyanov V, Wen X, de Silva JVL, Mironov V (2012) Nanotechnological strategies for biofabrication of human organs. J Nanotechnol 2012:149264
Miller JS, Steven KR, Yang MT, Baker BM, Nguyen D-HT, Cohen DM, Toro E, Chen AA, Galie PA, Yu X, Chaturvedi R, Bhatia SN, Chen CS (2012) Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 11:768
Nahmias Y, Schwartz RE, Verfaillie CM, Odde D (2005) Laser-guided direct writing for three-dimensional tissue engineering. Biotechnol Bioeng 92:129
Cruise GM, Scharp DS, Hubbell JA (1998) Characterization of permeability and network structure of interfacially photopolymerized poly(ethylene glycol) diacrylate hydrogels. Biomaterials 19:1287
Nguyen KT, West JL (2002) Photopolymerizable hydrogels for tissue engineering applications. Biomaterials 23:4307
Kim BC, Gu MB (2003) A bioluminescent sensor for high throughput toxicity classification. Biosens Bioelectron 18:1015
Andersen JB, Sternberg C, Poulsen L, Bjorn S, Givskov M, Molin S (1998) New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol 64:2240
Williams W, Cui W, Levchenko A, Stevens AM (2008) Robust and sensitive control of a quorum-sensing circuit by two interlocked feedback loops. Mol Syst Biol 4:234
Wu Y, Joseph S, Aluru NR (2009) Effect of cross-linking on the diffusion of water, ions, and small molecules in hydrogels. J Phys Chem B 113:3512
Adam M, Murali B, Glenn NO, Potter SS (2008) Epigenetic inheritance based evolution of antibiotic resistance in bacteria. BMC Evol Biol 8:52
Bierne H, Hamon M, Cossart P (2012) Epigenetics and bacterial infections. Cold Spring Harb Perspect Med 2:a010272
Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711
Duran-Pinedo AE, Paster B, Teles R, Frias-Lopez J (2011) Correlation network analysis applied to complex biofilm communities. PLoS One 6:e28438
Kolenbrander PE (2000) Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol 54:413
Margulies M, Eqholm M, Altman WE, Attaya S et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376
Hong P-Y, Hwang C, Ling F, Anderson GL, LeChevallier MW, Liu W-T (2010) Pyrosequencing analysis of bacterial biofilm communities in water meters of a drinking water distribution system. Appl Environ Microbiol 76:5631
Percival SL, Malic S, Cruz H, Williams DW (2011) Biofilms and veterinary medicine, vol 6, Springer series on biofilms. Springer, Berlin, pp 41–48
Baum MM, Kainović A, O’Keeffe T, Pandita R, McDonald K, Wu S, Webster P (2009) Characterization of structures in biofilms formed by a Pseudomonas fluorescens isolated from soil. BMC Microbiol 9:103
Thar R, KĂĽhil M (2002) Conspicuous veils formed by vibrioid bacteria on sulfidic marine sediment. Appl Environ Microbiol 68:6310
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
Wimpenny JWT, Colasanti R (1997) A unifying hypothesis for the structure of microbial biofilms based on cellular automaton models. FEMS Microbiol Ecol 22:1
Perry N, Nelson EM, Sarveswaran K, Kurz V, Timp G (2013) Wiring a biological integrated circuit (unpublished manuscript)
Seliktar D (2005) Extracellular stimulation in tissue engineering. Ann N Y Acad Sci 1047:386
Acknowledgments
We gratefully acknowledge support from NSF CCF-1129098. We are also grateful to R. Weiss for the donation of receiver plasmids and W-T Liu for sharing his preliminary sequencing data.
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Nelson, E.M. et al. (2015). Ecology of a Simple Synthetic Biofilm. In: Hagen, S. (eds) The Physical Basis of Bacterial Quorum Communication. Biological and Medical Physics, Biomedical Engineering. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1402-9_11
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DOI: https://doi.org/10.1007/978-1-4939-1402-9_11
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