Ecology of a Simple Synthetic Biofilm

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.

[1]  Brendon M. Baker,et al.  Rapid casting of patterned vascular networks for perfusable engineered 3D tissues , 2012, Nature materials.

[2]  J. Costerton,et al.  The involvement of cell-to-cell signals in the development of a bacterial biofilm. , 1998, Science.

[3]  Vladimir Mironov,et al.  Towards organ printing: engineering an intra-organ branched vascular tree , 2010, Expert opinion on biological therapy.

[4]  Ertugrul M. Ozbudak,et al.  Regulation of noise in the expression of a single gene , 2002, Nature Genetics.

[5]  Nicolas Perry,et al.  Epigenetic memory emerging from integrated transcription bursts. , 2013, Biophysical journal.

[6]  A. Kharazmi,et al.  Robbins device in biofilm research. , 1999, Methods in enzymology.

[7]  Gregory Timp,et al.  Jamming prokaryotic cell-to-cell communications in a model biofilm. , 2009, Lab on a chip.

[8]  M. Baum,et al.  Characterization of structures in biofilms formed by a Pseudomonas fluorescens isolated from soil , 2009, BMC Microbiology.

[9]  Man Bock Gu,et al.  A bioluminescent sensor for high throughput toxicity classification. , 2003, Biosensors & bioelectronics.

[10]  Sangeeta N Bhatia,et al.  Micromechanical control of cell–cell interactions , 2007, Proceedings of the National Academy of Sciences.

[11]  E. Greenberg,et al.  Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. , 2001, Annual review of genetics.

[12]  Sony Joseph,et al.  Effect of cross-linking on the diffusion of water, ions, and small molecules in hydrogels. , 2009, The journal of physical chemistry. B.

[13]  S. Potter,et al.  Epigenetic inheritance based evolution of antibiotic resistance in bacteria , 2008, BMC Evolutionary Biology.

[14]  Burkhard A. Hense,et al.  Does efficiency sensing unify diffusion and quorum sensing? , 2007, Nature Reviews Microbiology.

[15]  Jan Scrimgeour,et al.  Live cell lithography: using optical tweezers to create synthetic tissue. , 2008, Lab on a chip.

[16]  A. Goryachev,et al.  Systems analysis of a quorum sensing network: design constraints imposed by the functional requirements, network topology and kinetic constants. , 2006, Bio Systems.

[17]  P. Kolenbrander,et al.  Oral microbial communities: biofilms, interactions, and genetic systems. , 2000, Annual review of microbiology.

[18]  B. Iglewski,et al.  Bacterial Quorum Sensing in Pathogenic Relationships , 2000, Infection and Immunity.

[19]  David W Williams,et al.  Introduction to biofilms , 2011 .

[20]  K. Lewis,et al.  Riddle of Biofilm Resistance , 2001, Antimicrobial Agents and Chemotherapy.

[21]  Nicolas Perry,et al.  Biological noise abatement: coordinating the responses of autonomous bacteria in a synthetic biofilm to a fluctuating environment using a stochastic bistable switch. , 2014, ACS synthetic biology.

[22]  A. Levchenko,et al.  Robust and sensitive control of a quorum-sensing circuit by two interlocked feedback loops , 2008, Molecular systems biology.

[23]  S. C. Winans,et al.  Chemical communication in proteobacteria: biochemical and structural studies of signal synthases and receptors required for intercellular signalling , 2004, Molecular microbiology.

[24]  J. Wimpenny,et al.  A unifying hypothesis for the structure of microbial biofilms based on cellular automaton models , 1997 .

[25]  C. Rao,et al.  Control, exploitation and tolerance of intracellular noise , 2002, Nature.

[26]  Karoly Jakab,et al.  Tissue engineering by self-assembly and bio-printing of living cells , 2010, Biofabrication.

[27]  Michail Stamatakis,et al.  Comparison of deterministic and stochastic models of the lac operon genetic network. , 2009, Biophysical journal.

[28]  A. Arkin,et al.  Stochastic mechanisms in gene expression. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[29]  D. Seliktar,et al.  Extracellular Stimulation in Tissue Engineering , 2005, Annals of the New York Academy of Sciences.

[30]  B. Paster,et al.  Correlation Network Analysis Applied to Complex Biofilm Communities , 2011, PloS one.

[31]  J. Raser,et al.  Noise in Gene Expression: Origins, Consequences, and Control , 2005, Science.

[32]  B. Bassler,et al.  Quorum sensing in bacteria. , 2001, Annual review of microbiology.

[33]  M. Thattai,et al.  Stochastic Gene Expression in Fluctuating Environments , 2004, Genetics.

[34]  Pascale Cossart,et al.  Epigenetics and bacterial infections. , 2012, Cold Spring Harbor perspectives in medicine.

[35]  Mark W. LeChevallier,et al.  Pyrosequencing Analysis of Bacterial Biofilm Communities in Water Meters of a Drinking Water Distribution System , 2010, Applied and Environmental Microbiology.

[36]  L. Tsimring,et al.  A synchronized quorum of genetic clocks , 2009, Nature.

[37]  D. Stickler,et al.  Bacterial biofilms in patients with indwelling urinary catheters , 2008, Nature Clinical Practice Urology.

[38]  Paul Stoodley,et al.  The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities , 2006, Analytical and bioanalytical chemistry.

[39]  Vladimir Mironov,et al.  Nanotechnological Strategies for Biofabrication of Human Organs , 2012 .

[40]  A. Arkin,et al.  From Fluctuations to Phenotypes: The Physiology of Noise , 2006, Science's STKE.

[41]  H. Flemming,et al.  The biofilm matrix , 2010, Nature Reviews Microbiology.

[42]  P. Matsudaira,et al.  Laser-guided assembly of heterotypic three-dimensional living cell microarrays. , 2006, Biophysical journal.

[43]  Y. Nahmias,et al.  Laser-guided direct writing for three-dimensional tissue engineering. , 2005, Biotechnology and bioengineering.

[44]  Robert L Sah,et al.  Probing the role of multicellular organization in three-dimensional microenvironments , 2006, Nature Methods.

[45]  Paul Stoodley,et al.  Bacterial biofilms: from the Natural environment to infectious diseases , 2004, Nature Reviews Microbiology.

[46]  M. Kühl,et al.  Conspicuous Veils Formed by Vibrioid Bacteria on Sulfidic Marine Sediment , 2002, Applied and Environmental Microbiology.

[47]  Gordon Ramage,et al.  Candida biofilms on implanted biomaterials: a clinically significant problem. , 2006, FEMS yeast research.

[48]  Christian Chauret,et al.  Detection of Aeromonas hydrophila in a drinking-water distribution system: a field and pilot study. , 2001, Canadian journal of microbiology.

[49]  L. Poulsen,et al.  New Unstable Variants of Green Fluorescent Protein for Studies of Transient Gene Expression in Bacteria , 1998, Applied and Environmental Microbiology.

[50]  M. Ozkan,et al.  Electro-optical platform for the manipulation of live cells , 2003 .

[51]  J. Hubbell,et al.  Characterization of permeability and network structure of interfacially photopolymerized poly(ethylene glycol) diacrylate hydrogels. , 1998, Biomaterials.

[52]  Anne K Camper,et al.  Molecular interactions in biofilms. , 2002, Chemistry & biology.

[53]  R. Redfield Is quorum sensing a side effect of diffusion sensing? , 2002, Trends in microbiology.

[54]  James R. Knight,et al.  Genome sequencing in microfabricated high-density picolitre reactors , 2005, Nature.

[55]  D. Beer,et al.  Flowing biofilms as a transport mechanism for biomass through porous media under laminar and turbulent conditions in a laboratory reactor system , 2005, Biofouling.

[56]  C. Lévesque,et al.  Bacterial biofilm: structure, function, and antimicrobial resistance , 2010 .

[57]  Kytai Truong Nguyen,et al.  Photopolymerizable hydrogels for tissue engineering applications. , 2002, Biomaterials.

[58]  Holger Daims,et al.  Drivers of bacterial colonization patterns in stream biofilms. , 2010, FEMS microbiology ecology.

[59]  Steven L. Percival,et al.  Biofilms and Veterinary Medicine , 2011 .

[60]  Joe Tien,et al.  Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. , 2007, Lab on a chip.

[61]  A. Khademhosseini,et al.  A cell-laden microfluidic hydrogel. , 2007, Lab on a chip.

[62]  A. van Oudenaarden,et al.  Noise Propagation in Gene Networks , 2005, Science.

[63]  C. S. Chen,et al.  Geometric control of cell life and death. , 1997, Science.

[64]  Farren J. Isaacs,et al.  Phenotypic consequences of promoter-mediated transcriptional noise. , 2006, Molecular cell.