Biofilm streamers cause catastrophic disruption of flow with consequences for environmental and medical systems

Biofilms are antibiotic-resistant, sessile bacterial communities that occupy most moist surfaces on Earth and cause chronic and medical device-associated infections. Despite their importance, basic information about biofilm dynamics in common ecological environments is lacking. Here, we demonstrate that flow through soil-like porous materials, industrial filters, and medical stents dramatically modifies the morphology of Pseudomonas aeruginosa biofilms to form 3D streamers, which, over time, bridge the spaces between obstacles and corners in nonuniform environments. We discovered that accumulation of surface-attached biofilm has little effect on flow through such environments, whereas biofilm streamers cause sudden and rapid clogging. We demonstrate that flow-induced shedding of extracellular matrix from surface-attached biofilms generates a sieve-like network that captures cells and other biomass, which add to the existing network, causing exponentially fast clogging independent of growth. These results suggest that biofilm streamers are ubiquitous in nature and strongly affect flow through porous materials in environmental, industrial, and medical systems.

[1]  Thomas Bjarnsholt,et al.  Towards diagnostic guidelines for biofilm-associated infections. , 2012, FEMS immunology and medical microbiology.

[2]  C. Causserand,et al.  Formation of bacterial streamers during filtration in microfluidic systems , 2012, Biofouling.

[3]  Cristian Picioreanu,et al.  The effect of biofilm permeability on bio‐clogging of porous media , 2012, Biotechnology and bioengineering.

[4]  R. Geffers,et al.  The Pseudomonas aeruginosa Transcriptome in Planktonic Cultures and Static Biofilms Using RNA Sequencing , 2012, PloS one.

[5]  P. Stewart,et al.  Mini-review: Convection around biofilms , 2012, Biofouling.

[6]  F. Lépine,et al.  Active Starvation Responses Mediate Antibiotic Tolerance in Biofilms and Nutrient-Limited Bacteria , 2011, Science.

[7]  J. Dunkel,et al.  Fluid dynamics and noise in bacterial cell–cell and cell–surface scattering , 2011, Proceedings of the National Academy of Sciences.

[8]  Laura Guglielmini,et al.  Secondary flow as a mechanism for the formation of biofilm streamers. , 2011, Biophysical journal.

[9]  Renaud Escudié,et al.  Control of start-up and operation of anaerobic biofilm reactors: an overview of 15 years of research. , 2011, Water research.

[10]  Garth D Ehrlich,et al.  Physiology of Pseudomonas aeruginosa in biofilms as revealed by transcriptome analysis , 2010, BMC Microbiology.

[11]  Laura Guglielmini,et al.  Laminar flow around corners triggers the formation of biofilm streamers , 2010, Journal of The Royal Society Interface.

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

[13]  G. Donelli,et al.  Microbial biofilms associated with biliary stent clogging. , 2010, FEMS immunology and medical microbiology.

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

[15]  Qinjun Kang,et al.  Effects of pore-scale heterogeneity and transverse mixing on bacterial growth in porous media. , 2010, Environmental science & technology.

[16]  Carey D. Nadell,et al.  Emergence of Spatial Structure in Cell Groups and the Evolution of Cooperation , 2010, PLoS Comput. Biol..

[17]  Martin Thullner,et al.  Comparison of bioclogging effects in saturated porous media within one- and two-dimensional flow systems , 2010 .

[18]  Y. Pachepsky,et al.  Biofilm morphology as related to the porous media clogging. , 2010, Water research.

[19]  B. Bassler,et al.  Bacterial quorum-sensing network architectures. , 2009, Annual review of genetics.

[20]  M. Cámara,et al.  Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. , 2009, Current opinion in microbiology.

[21]  M. V. van Loosdrecht,et al.  Biofouling of spiral-wound nanofiltration and reverse osmosis membranes: a feed spacer problem. , 2009, Water research.

[22]  T. Tolker-Nielsen,et al.  Pattern formation in Pseudomonas aeruginosa biofilms. , 2008, Current opinion in microbiology.

[23]  C. Whitchurch,et al.  Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. , 2008, Environmental microbiology.

[24]  Philippe Baveye,et al.  Computational pore network modeling of the influence of biofilm permeability on bioclogging in porous media , 2008, Biotechnology and bioengineering.

[25]  Alkiviades C. Payatakes,et al.  Hierarchical simulator of biofilm growth and dynamics in granular porous materials , 2007 .

[26]  G. O’Toole,et al.  Roles for flagellar stators in biofilm formation by Pseudomonas aeruginosa. , 2007, Research in microbiology.

[27]  R. B. Jackson,et al.  Toward an ecological classification of soil bacteria. , 2007, Ecology.

[28]  R. Kolter,et al.  Quorum-Sensing Regulation of the Biofilm Matrix Genes (pel) of Pseudomonas aeruginosa , 2007, Journal of bacteriology.

[29]  P. Stewart,et al.  Spatial Patterns of DNA Replication, Protein Synthesis, and Oxygen Concentration within Bacterial Biofilms Reveal Diverse Physiological States , 2007, Journal of bacteriology.

[30]  J. Tay,et al.  Distribution of extracellular polymeric substances in aerobic granules , 2007, Applied Microbiology and Biotechnology.

[31]  Barbara J. Wold,et al.  Spatiometabolic Stratification of Shewanella oneidensis Biofilms , 2006, Applied and Environmental Microbiology.

[32]  R. Kolter,et al.  Microbial sciences: The superficial life of microbes , 2006, Nature.

[33]  T. Tolker-Nielsen,et al.  Growing and Analyzing Biofilms in Flow Cells , 2006, Current protocols in microbiology.

[34]  H. C. van der Mei,et al.  Microbial Adhesion in Flow Displacement Systems , 2006, Clinical Microbiology Reviews.

[35]  Hilmar Franke,et al.  Optically Transparent Porous Medium for Nondestructive Studies of Microbial Biofilm Architecture and Transport Dynamics , 2005, Applied and Environmental Microbiology.

[36]  B. Stevenson,et al.  Current Protocols in Microbiology , 2005 .

[37]  H. Schweizer,et al.  A Tn7-based broad-range bacterial cloning and expression system , 2005, Nature Methods.

[38]  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.

[39]  Roberto Kolter,et al.  Biofilms: the matrix revisited. , 2005, Trends in microbiology.

[40]  Lotte Lambertsen,et al.  Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins. , 2004, Environmental microbiology.

[41]  T. L. Stewart,et al.  Modeling of biomass-plug development and propagation in porous media , 2004 .

[42]  Roberto Kolter,et al.  Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms , 2003, Molecular microbiology.

[43]  P. Stewart,et al.  A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance , 2003, Nature.

[44]  Søren Molin,et al.  Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms , 2003, Molecular microbiology.

[45]  D. Allison,et al.  The Biofilm Matrix , 2003, Biofouling.

[46]  Jost Wingender,et al.  Application of fluorescently labelled lectins for the visualization and biochemical characterization of polysaccharides in biofilms of Pseudomonas aeruginosa. , 2002, Journal of microbiological methods.

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

[48]  J. Mattick,et al.  Extracellular DNA required for bacterial biofilm formation. , 2002, Science.

[49]  J. Costerton,et al.  Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm , 2002, Journal of bacteriology.

[50]  Derick G. Brown,et al.  Effects of porous media preparation on bacteria transport through laboratory columns. , 2002, Water research.

[51]  Peter K. Kitanidis,et al.  Pore‐scale modeling of biological clogging due to aggregate expansion: A material mechanics approach , 2001 .

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

[53]  S. Quake,et al.  Monolithic microfabricated valves and pumps by multilayer soft lithography. , 2000, Science.

[54]  R. Kolter,et al.  Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development , 1998, Molecular microbiology.

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

[56]  J J Heijnen,et al.  Mathematical modeling of biofilm structure with a hybrid differential-discrete cellular automaton approach. , 1998, Biotechnology and bioengineering.

[57]  Z Lewandowski,et al.  Oscillation characteristics of biofilm streamers in turbulent flowing water as related to drag and pressure drop. , 1998, Biotechnology and bioengineering.

[58]  S. Silver Pseudomonas aeruginosa as an opportunistic pathogen , 1994 .

[59]  K. Botzenhart,et al.  Ecology and Epidemiologyof Pseudomonas aeruginosa , 1993 .

[60]  M Lanzer,et al.  Promoters largely determine the efficiency of repressor action. , 1988, Proceedings of the National Academy of Sciences of the United States of America.