Global gene expression in Escherichia coli biofilms

It is now apparent that microorganisms undergo significant changes during the transition from planktonic to biofilm growth. These changes result in phenotypic adaptations that allow the formation of highly organized and structured sessile communities, which possess enhanced resistance to antimicrobial treatments and host immune defence responses. Escherichia coli has been used as a model organism to study the mechanisms of growth within adhered communities. In this study, we use DNA microarray technology to examine the global gene expression profile of E. coli during sessile growth compared with planktonic growth. Genes encoding proteins involved in adhesion (type 1 fimbriae) and, in particular, autoaggregation (Antigen 43) were highly expressed in the adhered population in a manner that is consistent with current models of sessile community development. Several novel gene clusters were induced upon the transition to biofilm growth, and these included genes expressed under oxygen‐limiting conditions, genes encoding (putative) transport proteins, putative oxidoreductases and genes associated with enhanced heavy metal resistance. Of particular interest was the observation that many of the genes altered in expression have no current defined function. These genes, as well as those induced by stresses relevant to biofilm growth such as oxygen and nutrient limitation, may be important factors that trigger enhanced resistance mechanisms of sessile communities to antibiotics and hydrodynamic shear forces.

[1]  H. Hasman,et al.  Antigen-43-Mediated Autoaggregation ofEscherichia coli Is Blocked by Fimbriation , 1999, Journal of bacteriology.

[2]  S. Møller,et al.  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 , 1996, Applied and environmental microbiology.

[3]  B. Christensen,et al.  Establishment of New Genetic Traits in a Microbial Biofilm Community , 1998, Applied and Environmental Microbiology.

[4]  M. Schembri,et al.  Coordinate gene regulation by fimbriae‐induced signal transduction , 2001, The EMBO journal.

[5]  M. Schembri,et al.  FimH‐mediated autoaggregation of Escherichia coli , 2001, Molecular microbiology.

[6]  R. Hengge-aronis,et al.  The role of the sigma factor sigma S (KatF) in bacterial global regulation. , 1994, Annual review of microbiology.

[7]  C. Prigent-Combaret,et al.  Abiotic Surface Sensing and Biofilm-Dependent Regulation of Gene Expression in Escherichia coli , 1999, Journal of bacteriology.

[8]  Dong-Eun Chang,et al.  Gene expression profiling of Escherichia coli growth transitions: an expanded stringent response model , 2002, Molecular microbiology.

[9]  R. Kolter,et al.  Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili , 1998, Molecular microbiology.

[10]  G. Phillips.  New cloning vectors with temperature-sensitive replication. , 1999, Plasmid.

[11]  Mark A. Schembri,et al.  Antigen 43 and Type 1 Fimbriae Determine Colony Morphology of Escherichia coli K-12 , 2000, Journal of bacteriology.

[12]  F. Blattner,et al.  Functional Genomics: Expression Analysis ofEscherichia coli Growing on Minimal and Rich Media , 1999, Journal of bacteriology.

[13]  C. Dorman,et al.  Control of Escherichia coli type 1 fimbrial gene expression in stationary phase: a negative role for RpoS , 1997, Molecular and General Genetics MGG.

[14]  Chiara Sabatti,et al.  Co-expression pattern from DNA microarray experiments as a tool for operon prediction , 2002, Nucleic Acids Res..

[15]  Robert L. Campbell,et al.  ESCHERICHIA COLI K-12* , 1973 .

[16]  R. Hengge-aronis,et al.  Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S , 1991, Journal of bacteriology.

[17]  F. Neidhardt,et al.  Culture Medium for Enterobacteria , 1974, Journal of bacteriology.

[18]  K. Otto,et al.  Adhesion of Type 1-Fimbriated Escherichia coli to Abiotic Surfaces Leads to Altered Composition of Outer Membrane Proteins , 2001, Journal of bacteriology.

[19]  G. Church,et al.  RNA expression analysis using a 30 base pair resolution Escherichia coli genome array , 2000, Nature Biotechnology.

[20]  M. Schembri,et al.  Bacterial adhesins: function and structure. , 2000, International journal of medical microbiology : IJMM.

[21]  P. Sereno,et al.  The evolution of dinosaurs. , 1999, Science.

[22]  R. McLean,et al.  Impact of rpoS Deletion onEscherichia coli Biofilms , 1999, Applied and Environmental Microbiology.

[23]  R. Gunsalus,et al.  Effect of microaerophilic cell growth conditions on expression of the aerobic (cyoABCDE and cydAB) and anaerobic (narGHJI, frdABCD, and dmsABC) respiratory pathway genes in Escherichia coli , 1996, Journal of bacteriology.

[24]  T. Caldas,et al.  Chaperone Properties of the Bacterial Periplasmic Substrate-binding Proteins* , 1997, The Journal of Biological Chemistry.

[25]  M. W. van der Woude,et al.  Phase variation of Ag43 in Escherichia coli: Dam‐dependent methylation abrogates OxyR binding and OxyR‐mediated repression of transcription , 2000, Molecular microbiology.

[26]  N. W. Davis,et al.  The complete genome sequence of Escherichia coli K-12. , 1997, Science.

[27]  D. Ussery,et al.  DNA microarray analysis of fim mutations in Escherichia coli , 2002, Molecular Genetics and Genomics.

[28]  Frederick R. Blattner,et al.  High-Density Microarray-Mediated Gene Expression Profiling of Escherichia coli , 2001, Journal of bacteriology.

[29]  M. Givskov,et al.  An Attractive Surface: Gram-Negative Bacterial Biofilms , 2002, Science's STKE.

[30]  C. Prigent-Combaret,et al.  Complex Regulatory Network Controls Initial Adhesion and Biofilm Formation in Escherichia coli via Regulation of thecsgD Gene , 2001, Journal of bacteriology.

[31]  Roger E. Bumgarner,et al.  Gene expression in Pseudomonas aeruginosa biofilms , 2001, Nature.

[32]  J. Costerton,et al.  Bacterial biofilms: a common cause of persistent infections. , 1999, Science.

[33]  R. Kolter,et al.  Biofilm formation as microbial development. , 2000, Annual review of microbiology.

[34]  A. Tsygankov,et al.  Effect of O2, H2 and redox potential on the activity and synthesis of hydrogenase 2 in Escherichia coli. , 2001, Research in microbiology.

[35]  I. Henderson,et al.  The Major Phase-Variable Outer Membrane Protein ofEscherichia coli Structurally Resembles the Immunoglobulin A1 Protease Class of Exported Protein and Is Regulated by a Novel Mechanism Involving Dam and OxyR , 1999, Journal of bacteriology.

[36]  R. Sparling,et al.  Regulation in the rpoS regulon of Escherichia coli. , 1998, Canadian journal of microbiology.

[37]  S. Molin,et al.  Spatial Organization of Microbial Biofilm Communities , 2000, Microbial Ecology.

[38]  P. Klemm,et al.  Localization of promoters in the fim gene cluster and the effect of H-NS on the transcription of fimB and fimE. , 1994, FEMS microbiology letters.

[39]  M. Schembri,et al.  Biofilm Formation in a Hydrodynamic Environment by Novel FimH Variants and Ramifications for Virulence , 2001, Infection and Immunity.

[40]  J. Costerton,et al.  Antibiotic resistance of bacteria in biofilms , 2001, The Lancet.

[41]  S. Molin,et al.  Antigen 43 facilitates formation of multispecies biofilms. , 2000, Environmental microbiology.

[42]  H. Hasman,et al.  Antigen 43 from Escherichia coli Induces Inter- and Intraspecies Cell Aggregation and Changes in Colony Morphology of Pseudomonas fluorescens , 2000, Journal of bacteriology.

[43]  J. Costerton,et al.  Biofilms: Survival Mechanisms of Clinically Relevant Microorganisms , 2002, Clinical Microbiology Reviews.