Physicochemical regulation of biofilm formation

This article reviews the physical and chemical constraints of environments on biofilm formation. We provide a perspective on how materials science and engineering can address fundamental questions and unmet technological challenges in this area of microbiology, such as biofilm prevention. Specifically, we discuss three factors that impact the development and organization of bacterial communities. (1) Physical properties of surfaces regulate cell attachment and physiology and affect early stages of biofilm formation. (2) Chemical properties influence the adhesion of cells to surfaces and their development into biofilms and communities. (3) Chemical communication between cells attenuates growth and influences the organization of communities. Mechanisms of spatial and temporal confinement control the dimensions of communities and the diffusion path length for chemical communication between biofilms, which, in turn, influences biofilm phenotypes. Armed with a detailed understanding of biofilm formation, researchers are applying the tools and techniques of materials science and engineering to revolutionize the study and control of bacterial communities growing at interfaces.

[1]  Elena P. Ivanova,et al.  Effect of ultrafine-grained titanium surfaces on adhesion of bacteria , 2009, Applied Microbiology and Biotechnology.

[2]  Xingyu Jiang,et al.  Palladium as a substrate for self-assembled monolayers used in biotechnology. , 2004, Analytical chemistry.

[3]  G. Wong,et al.  Synthetic antimicrobial oligomers induce a composition-dependent topological transition in membranes. , 2007, Journal of the American Chemical Society.

[4]  J. Costerton,et al.  Bacterial biofilms in nature and disease. , 1987, Annual review of microbiology.

[5]  K. V. Van Vliet,et al.  Substrata mechanical stiffness can regulate adhesion of viable bacteria. , 2008, Biomacromolecules.

[6]  J. A. V. BUTLER,et al.  Theory of the Stability of Lyophobic Colloids , 1948, Nature.

[7]  P. G. de Gennes,et al.  Polymers at an interface; a simplified view , 1987 .

[8]  James M. Anderson,et al.  S. epidermidis biofilm formation: effects of biomaterial surface chemistry and serum proteins. , 2007, Journal of biomedical materials research. Part A.

[9]  H. Ohshima Electrophoretic mobility of soft particles , 1995 .

[10]  C. R. Lowe,et al.  Optimisation of polymeric surface pre‐treatment to prevent bacterial biofilm formation for use in microfluidics , 2004, Journal of molecular recognition : JMR.

[11]  T. Tolker-Nielsen,et al.  An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. , 2010, FEMS immunology and medical microbiology.

[12]  G. Wong,et al.  Mechanism of a prototypical synthetic membrane-active antimicrobial: Efficient hole-punching via interaction with negative intrinsic curvature lipids , 2008, Proceedings of the National Academy of Sciences.

[13]  A. Gristina,et al.  Biomaterial-centered infection: microbial adhesion versus tissue integration. , 1987, Science.

[14]  Joanna Aizenberg,et al.  Bacteria pattern spontaneously on periodic nanostructure arrays. , 2010, Nano letters.

[15]  C Jeffrey Brinker,et al.  Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. , 2010, Nature chemical biology.

[16]  Michael Wagner,et al.  Reversible and Irreversible Adhesion of Motile Escherichia coli Cells Analyzed by Total Internal Reflection Aqueous Fluorescence Microscopy , 2002, Applied and Environmental Microbiology.

[17]  J. Pringle,et al.  Influence of Substratum Wettability on Attachment of Freshwater Bacteria to Solid Surfaces , 1983, Applied and environmental microbiology.

[18]  A. Klibanov,et al.  Bactericidal and virucidal ultrathin films assembled layer by layer from polycationic N-alkylated polyethylenimines and polyanions. , 2010, Biomaterials.

[19]  G. Wong,et al.  Mechanism of A Prototypical Synthetic Membrane-Active Antimicrobial: Efficient Hole-Punching by Targeting Lipids With Negative Spontaneous Curvature Lipids , 2008 .

[20]  A. Wolfe,et al.  A Complex Transcription Network Controls the Early Stages of Biofilm Development by Escherichia coli , 2006, Journal of bacteriology.

[21]  A. Ulman,et al.  Formation and Structure of Self-Assembled Monolayers. , 1996, Chemical reviews.

[22]  C. R. Arciola,et al.  Study of Staphylococcus Aureus Adhesion on a Novel Nanostructured Surface by Chemiluminometry , 2006, The International journal of artificial organs.

[23]  R. Knight,et al.  The Human Microbiome Project , 2007, Nature.

[24]  A. Klibanov,et al.  On structural damage incurred by bacteria upon exposure to hydrophobic polycationic coatings , 2011, Biotechnology Letters.

[25]  Derick G. Brown,et al.  Electrostatic behavior of the charge-regulated bacterial cell surface. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[26]  Mark H Schoenfisch,et al.  Reducing implant-related infections: active release strategies. , 2006, Chemical Society reviews.

[27]  J. Seymour,et al.  Biopolymer and water dynamics in microbial biofilm extracellular polymeric substance. , 2008, Biomacromolecules.

[28]  Y. Missirlis,et al.  Interactions of bacteria with specific biomaterial surface chemistries under flow conditions. , 2010, Acta biomaterialia.

[29]  M. Möller,et al.  Surface Coating Strategies to Prevent Biofilm Formation on Implant Surfaces , 2010 .

[30]  G. Whitesides,et al.  Microfabrication meets microbiology , 2007, Nature Reviews Microbiology.

[31]  G. Whitesides,et al.  Self-assembled monolayers of thiolates on metals as a form of nanotechnology. , 2005, Chemical reviews.

[32]  E. Kramarsky-Winter,et al.  Conditioning film and initial biofilm formation on ceramics tiles in the marine environment. , 2007, FEMS microbiology letters.

[33]  A. Mayes,et al.  Ultrafiltration membranes incorporating amphiphilic comb copolymer additives prevent irreversible adhesion of bacteria. , 2010, Environmental science & technology.

[34]  D. Weibel,et al.  Fabrication of microbial biofilm arrays by geometric control of cell adhesion. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[35]  Diane Hoffman-Kim,et al.  Topography, cell response, and nerve regeneration. , 2010, Annual review of biomedical engineering.

[36]  Shaoyi Jiang,et al.  A switchable biocompatible polymer surface with self-sterilizing and nonfouling capabilities. , 2008, Angewandte Chemie.

[37]  Christopher J. Long,et al.  Engineered nanoforce gradients for inhibition of settlement (attachment) of swimming algal spores. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[38]  James F. Schumacher,et al.  Impact of engineered surface microtopography on biofilm formation of Staphylococcus aureus , 2007, Biointerphases.

[39]  X. Wen,et al.  Biomaterial Strategies to Reduce Implant-Associated Infections , 2007, The International journal of artificial organs.

[40]  Eileen M. Spain,et al.  Spring constants and adhesive properties of native bacterial biofilm cells measured by atomic force microscopy. , 2008, Colloids and surfaces. B, Biointerfaces.

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

[42]  R. Baier Applied Chemistry at Protein Interfaces , 1975 .

[43]  Rustem F Ismagilov,et al.  Complex function by design using spatially pre-structured synthetic microbial communities: degradation of pentachlorophenol in the presence of Hg(ii). , 2011, Integrative biology : quantitative biosciences from nano to macro.

[44]  Alexander M Klibanov,et al.  Surpassing nature: rational design of sterile-surface materials. , 2005, Trends in biotechnology.

[45]  R. Ismagilov,et al.  Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. , 2009, Angewandte Chemie.

[46]  T. Webster,et al.  Nanotechnology: Pediatric Applications , 2010, Pediatric Research.

[47]  K. Young The Selective Value of Bacterial Shape , 2006, Microbiology and Molecular Biology Reviews.

[48]  M. Silverman,et al.  Surface‐induced swarmer cell differentiation of Vibrio parahaemoiyticus , 1990, Molecular microbiology.

[49]  Rustem F Ismagilov,et al.  Microfluidic stochastic confinement enhances analysis of rare cells by isolating cells and creating high density environments for control of diffusible signals. , 2010, Chemical Society reviews.

[50]  G. López,et al.  Attachment and detachment of bacteria on surfaces with tunable and switchable wettability , 2010, Biofouling.

[51]  G. López,et al.  Attachment of bacteria to model solid surfaces: oligo(ethylene glycol) surfaces inhibit bacterial attachment. , 1996, FEMS microbiology letters.

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

[53]  D. Weibel,et al.  Bacterial Swarming: A Model System for Studying Dynamic Self-assembly. , 2009, Soft matter.

[54]  Bao-Lian Su,et al.  Superhydrophobic surfaces: from natural to biomimetic to functional. , 2011, Journal of colloid and interface science.

[55]  M. C. Stuart,et al.  Sweet brushes and dirty proteins. , 2007, Soft matter.

[56]  J. Foster,et al.  Effects of gut microbiota on the brain: implications for psychiatry. , 2009, Journal of psychiatry & neuroscience : JPN.

[57]  Viola Vogel,et al.  Shear‐dependent ‘stick‐and‐roll’ adhesion of type 1 fimbriated Escherichia coli , 2004, Molecular microbiology.

[58]  W. Zingg,et al.  Surface thermodynamics of bacterial adhesion , 1983, Applied and environmental microbiology.

[59]  Roseanne M. Ford,et al.  Reversal of Flagellar Rotation Is Important in Initial Attachment of Escherichia coli to Glass in a Dynamic System with High- and Low-Ionic-Strength Buffers , 2002, Applied and Environmental Microbiology.

[60]  R. L. Wu,et al.  Prolonged control of patterned biofilm formation by bio-inert surface chemistry. , 2009, Chemical communications.

[61]  Ali Beskok,et al.  Zeta Potential of Selected Bacteria in Drinking Water When Dead, Starved, or Exposed to Minimal and Rich Culture Media , 2007, Current Microbiology.

[62]  Bharat Bhushan,et al.  Micro-, nano- and hierarchical structures for superhydrophobicity, self-cleaning and low adhesion , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[63]  Lee Makowski,et al.  Structural polymorphism of bacterial adhesion pili , 1995, Nature.

[64]  Jianzhu Chen,et al.  Polymeric coatings that inactivate both influenza virus and pathogenic bacteria , 2006, Proceedings of the National Academy of Sciences.

[65]  Jacob N. Israelachvili,et al.  Intermolecular and surface forces : with applications to colloidal and biological systems , 1985 .

[66]  J. Hubbell,et al.  Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering , 2005, Nature Biotechnology.

[67]  L. Ista,et al.  Surface-Grafted, Environmentally Sensitive Polymers for Biofilm Release , 1999, Applied and Environmental Microbiology.

[68]  M. E. Buck,et al.  Chemical modification of reactive multilayered films fabricated from poly(2-alkenyl azlactone)s: design of surfaces that prevent or promote mammalian cell adhesion and bacterial biofilm growth. , 2009, Biomacromolecules.

[69]  R. Seidu,et al.  Virus removal by unsaturated wastewater filtration: effects of biofilm accumulation and hydrophobicity. , 2009, Water science and technology : a journal of the International Association on Water Pollution Research.

[70]  R. Samudrala,et al.  Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix , 2010, Molecular microbiology.

[71]  W. Norde,et al.  My voyage of discovery to proteins in flatland ...and beyond. , 2008, Colloids and surfaces. B, Biointerfaces.

[72]  M. Elimelech,et al.  Role of type 1 fimbriae and mannose in the development of Escherichia coli K12 biofilm: from initial cell adhesion to biofilm formation , 2009, Biofouling.

[73]  W. Norde,et al.  Tethered polymer chains: surface chemistry and their impact on colloidal and surface properties. , 2003, Advances in colloid and interface science.

[74]  L Ploux,et al.  The interaction of cells and bacteria with surfaces structured at the nanometre scale. , 2010, Acta biomaterialia.

[75]  D. M. Lynn,et al.  Surface-mediated release of a synthetic small-molecule modulator of bacterial quorum sensing: gradual release enhances activity. , 2011, Chemical communications.

[76]  Karen A. Simon,et al.  Molecular gradients of bioinertness reveal a mechanistic difference between mammalian cell adhesion and bacterial biofilm formation. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[77]  J. Choi,et al.  Defined spatial structure stabilizes a synthetic multispecies bacterial community , 2008, Proceedings of the National Academy of Sciences.

[78]  W. Dunne,et al.  Bacterial Adhesion: Seen Any Good Biofilms Lately? , 2002, Clinical Microbiology Reviews.