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

Abstract

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 sievelike 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.bioclogging | biofouling | porous media I n the laboratory, bacteria are usually grown as planktonic cells in shaken suspensions, which differs dramatically from the natural environments of most microbes. In their natural habitats, bacteria often live in biofilms (1-3), which are tightly packed, surface-associated assemblies of bacteria that are bound together by extracellular polymeric substances (4, 5). Although biofilms are desirable in waste-water treatment (6), biofilms primarily cause undesirable effects such as chronic infections or clogging of industrial flow systems (1-3). Cells in biofilms display many behavioral differences from planktonic cells, such as a 1,000-fold increase in tolerance to antibiotics (7,8), an altered transcriptome (9-11), and spatially heterogeneous metabolic activity (12, 13). Some of these physiological peculiarities of biofilm-dwelling cells may be due to strong gradients of nutrients and metabolites, which also affect biofilm morphology and composition (14, 15). However, little is known about how physical aspects of the environment affect biofilm dynamics.The opportunistic pathogen Pseudomonas aeruginosa has become a model organism for biofilm studies largely because it forms biofilms in diverse habitats, including soil, rivers, sewage, and medical devices in humans (1, 2, 16). Two features are common to all of these environments: First, the presence of rough surfaces, which at the microscopic level reduce to surfaces with many corners, and second, a pressure-driven flow. The standard assay for growing biofilms in the laboratory abstracts from these realistic environments by typically using a smooth surface as a substrate, and either no flow or a pump to force nutritious medium across the biofilm at a constant flow rate (17-19). These standard assays have enabled the identification of several genes involved in biofilm develo...

A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation

“…Beyond being a clinically relevant pathogen, P. aeruginosa is an industrial and medical nuisance because it causes blockages in filtration devices and stents. P. aeruginosa PA14 also clogs microfluidic chambers that model such devices (26). Clogging is due to biofilms that produce exopolysaccharide-containing streamers that act as sieves to catch passing cells (26).…”

“…P. aeruginosa PA14 also clogs microfluidic chambers that model such devices (26). Clogging is due to biofilms that produce exopolysaccharide-containing streamers that act as sieves to catch passing cells (26). Compared with WT, lasR and rhlR single and double null mutants exhibit dramatically delayed clogging, demonstrating that quorum sensing is required to form blockages (Fig.…”

Dynamics of Bacterial Aggregates in Microflows

“…Flow effects are felt by a biofilm on much shorter time scales (seconds) than growth effects (hours) [4]. Biomass attaches, detaches and moves according to the flow fields at each location.…”

Bacterial predator–prey dynamics in microscale patchy landscapes

“…Over the past few years, microfabrication techniques have allowed for the creation of microscale synthetic ecosystems that are structured at the spatial scales relevant to bacterial populations [17][18][19][20][21]. It thus has become technically feasible to quantify bacterial predator-prey interactions in each of the individual micrometre-scale patches of a landscape under controlled conditions over many generations.…”