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Bacterial biofilms: from the Natural environment to infectious diseases

Key Points

  • Biofilms are clusters of microorganisms that stick to non-biological surfaces, such as rocks in a stream, as well as to surfaces on plants (roots) or in animals (epithelium).

  • These clusters are often encased in an outer polymer layer that can be produced by the microorganism or by the defensive mechanisms of the colonized host.

  • Biofilm formation is astonishingly widespread in nature and appears very early in the fossil record. Biofilm development also occurs in a vastly diverse range of microorganisms, including those that have changed little over of time. So, biofilm formation seems to be an ancient and fundamental part of the life cycles of many microorganisms and essential for survival in diverse environments.

  • Biofilm formation represents a protected mode of growth that not only allows cells to survive in hostile environments, but also to colonize new niches by dispersal of microorganisms from the microbial clusters.

  • Biofilms are an important, but incompletely understood, form of growth and survival for many bacteria. Recent evidence reveals that biofilms are structurally complex, dynamic systems that have both the characteristics of primitive multicellularly organized organisms and complex ecosystems.

  • In this review, the implications of survival and dispersal mechanisms are discussed in the context of both the natural environment and infectious diseases.

Abstract

Biofilms — matrix-enclosed microbial accretions that adhere to biological or non-biological surfaces — represent a significant and incompletely understood mode of growth for bacteria. Biofilm formation appears early in the fossil record (3.25 billion years ago) and is common throughout a diverse range of organisms in both the Archaea and Bacteria lineages, including the 'living fossils' in the most deeply dividing branches of the phylogenetic tree. It is evident that biofilm formation is an ancient and integral component of the prokaryotic life cycle, and is a key factor for survival in diverse environments. Recent advances show that biofilms are structurally complex, dynamic systems with attributes of both primordial multicellular organisms and multifaceted ecosystems. Biofilm formation represents a protected mode of growth that allows cells to survive in hostile environments and also disperse to colonize new niches. The implications of these survival and propagative mechanisms in the context of both the natural environment and infectious diseases are discussed in this review.

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Figure 1: Conceptualization of biofilm development and dynamic behaviours.
Figure 2: Structural similarity of biofilms growing in hydrothermal hot springs, freshwater rivers and laboratory flow cells.
Figure 3: Staphylococcus aureus biofilms.
Figure 4: Schematic showing three examples of possible points of entry into the body for infectious biofilms; catheter, hip replacement, and periodontal disease.

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Financial support was provided by the National Institutes of Health.

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DATABASES

Entrez

Escherichia coli

Pseudomonas aeruginosa

FURTHER INFORMATION

biofilm movies

web-based version of Figure 1

Glossary

BIOFILM

Microbial biofilms are populations of microorganisms that are concentrated at an interface (usually solid–liquid) and typically surrounded by an extracellular polymeric substance (EPS) matrix. Aggregates of cells not attached to a surface are sometimes termed 'flocs' and have many of the same characteristics as biofilms.

PLANKTONIC CELLS

Planktonic (or suspended) cell cultures are those grown primarily as single cells in suspension, either in a chemostat or a shake flask.

SESSILE

In an ecological context, a stationary organism such as a plant or a barnacle. In biofilm microbiology, it is used to distinguish planktonic (free-floating) prokaryotic cells from those attached to surfaces. However, new evidence shows that these 'sessile' cells are often dynamic, at least on the microscopic scale.

STREAMERS

Filamentous biofilm microcolonies that form in flowing water. The streamers are atached to the surface by an upstream 'head', while the downstream 'tail' can oscillate in the current.

PERIPHYTON

An assemblage of organisms attached to and living on submerged solid surfaces in natural environments such as rivers.

STROMATOLITE

Mushroom- and tower-shaped structures formed by layers of cyanobacteria and entrapped sediments that grow in quiescent (calm) saline and hydrothermal waters.

MASS TRANSFER

In the context of biofilms, mass transfer refers to the process by which dissolved and particulate substances (such as nutrients) are moved into and out of the biofilm by the surrounding fluid.

ADHESION

A stable interaction of a cell with respect to a surface. Living cells actively excrete chemicals from their surface to anchor themselves to a substratum. This is referred to as adhesion or attachment.

TYPE IV PILUS

An elongated structure extending from the surface of Gram-negative cells that is independent of flagella and which can retract and pull the cell forward.

DETACHMENT

The loss of single cells or aggregates of cells from the biofilm, usually into an overlying flow of fluid. Detachment can be an active process (dispersal), a passively induced mechanical process (for example, through fluid shear) or a chemical process (by adding agents that 'dissolve' the EPS matrix).

FLUID SHEAR

The mechanical force that is exerted by a fluid as it moves past a surface. Although shear exists throughout the fluid in biofilms, 'shear stress' is usually used in the context of the shear exerted at the solid surface — for example, where the biofilm is growing. The shear stress will tend to 'wash away' the attached biofilm from the surface on which it is growing, and it increases as the flow rate is increased.

EPS

Extracellular polymeric substance. Polymers of varying chemical composition that are excreted by the cells in the biofilm. The EPS is the slime matrix that gives the biofilm stability and helps it to adhere to a surface. Although generally assumed to be primarily composed of polysaccharides, the EPS can also contain proteins and nucleic acids.

ALGINATE

An exopolysaccharide produced by P. aeruginosa, which is believed to contribute to the antibiotic resistance of P. aeruginosa.

GLIDING OR TWITCHING MOTILITY

Movement, predominantly by Gram-negative cells, that is dependent on type IV pili.

VISCOELASTIC

A material that has both elastic (solid-like) and viscous (liquid-like) properties.

HYDROGELS

An extremely hydrated polymer gel. The polymer chain holds many times its weight in trapped water.

PERITRICHOUS FIMBRIAE

The many short extracellular pili appendages that protrude from the surface of some prokaryotic cells. Fimbriae are used for attachment to surfaces.

QUORUM SENSING

A system by which bacteria communicate. Signalling molecules — chemicals similar to pheromones that are produced by an individual bacterium — can affect the behaviour of surrounding bacteria.

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Hall-Stoodley, L., Costerton, J. & Stoodley, P. Bacterial biofilms: from the Natural environment to infectious diseases. Nat Rev Microbiol 2, 95–108 (2004). https://doi.org/10.1038/nrmicro821

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