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Chapter 1 : A Short History of the Development of the Biofilm Concept

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Abstract:

The development of the biofilm concept was a very gradual process, consisting of many small perceptions, which have now combined and synthesized and formed a significant “wave” that will carry microbiology far into the new millennium. Dozens of new methods have emerged that allow us to study bacteria where they actually live and carry out their roles as members of complex biofilm communities. Corrosion control is now increasingly based on the detection and control of biofilm populations. The objective of the early biofilm researchers was to locate and quantitate bacteria in various ecosystems and then to use basically morphological techniques to describe how they formed functional consortia within highly protected sessile communities. The imperative that drove early medical biofilm microbiology was the emergence of device-related and other chronic bacterial infections and the inability of the infectious disease community to control these infections or to explain their refractory nature. The modern era of biofilm research really began when Doug Caldwell's group introduced us to the confocal scanning laser microscope, with its ability to examine living hydrated specimens on opaque surfaces, at the fifth International Society for Microbial Ecology meeting in Osaka. One must always remember that all the methods used in monitoring gene expression in biofilms are "averaging," just as they are in planktonic cultures, and they tell us if the gene is up-regulated in some cells, but they do not tell us which cells or where they are located.

Citation: William Costerton J. 2004. A Short History of the Development of the Biofilm Concept, p 4-19. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch1
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Image of FIGURE 1
FIGURE 1

TEM of a section of embedded rumen contents, showing the phenomenal complexity of the cell envelopes and capsules of most of the bacterial cells in this natural population. These multilayered concentric structures have never been seen in the cell envelopes of rumen bacteria cultivated as planktonic cells in monospecies liquid cultures.

Citation: William Costerton J. 2004. A Short History of the Development of the Biofilm Concept, p 4-19. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch1
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Image of FIGURE 2
FIGURE 2

TEM of a section of embedded rumen contents showing the colonization of a cellulose fiber (F) by a biofilm composed of a single morphotype of a primary cellulose-degrading bacterium, which has attracted several spiral treponemes into the adjoining area. The cellulolytic activity of primary organisms has been shown to be increased because of end product (butyrate) removal by the treponemes in two-species pure culture experiments.

Citation: William Costerton J. 2004. A Short History of the Development of the Biofilm Concept, p 4-19. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch1
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Image of FIGURE 3
FIGURE 3

TEM of a section from the gut of a calf infected with the ETEC strain of to produce a model infection of “scours.” Note that the bacterial cells, which have remained associated with the microvillar surface during dozens of preparative washes, lie between 0.5 and 2.0 μm away from the tissue surface.

Citation: William Costerton J. 2004. A Short History of the Development of the Biofilm Concept, p 4-19. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch1
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Image of FIGURE 4
FIGURE 4

TEM of a section from the same animal as that seen in Fig. 3 , except that the specimen had been treated with ruthenium red during the fixation procedure. This acid polysaccharide-specific stain has revealed the presence of a very extensive glycocalyx surrounding each bacterial cell, which occupies the intervening space between the bacteria and the tissue and mediates the adhesion of the pathogen to the affected microvilli.

Citation: William Costerton J. 2004. A Short History of the Development of the Biofilm Concept, p 4-19. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch1
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Image of FIGURE 5
FIGURE 5

TEM of a section of a methacrylate slab that had been immersed in a mountain stream for 30 min, then “faced” with more methacrylate, and fixed and stained with ruthenium red. Note the formation of a single-cell biofilm in which cells of the predominant species ( are surrounded by matrix material, within which electron-dense clay platelets are also embedded.

Citation: William Costerton J. 2004. A Short History of the Development of the Biofilm Concept, p 4-19. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch1
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Image of FIGURE 6
FIGURE 6

Scanning electron micrograph of the lumenal surface of a Foley catheter recovered from a patient in whom it had formed the nidus of a catheter-associated urinary tract infection. Large numbers of cells of the infecting organism ( are seen to be embedded in matrix material that has been condensed in part by the dehydration necessary for scanning electron micrograph observations.

Citation: William Costerton J. 2004. A Short History of the Development of the Biofilm Concept, p 4-19. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch1
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Image of FIGURE 7
FIGURE 7

TEM of a ruthenium red-stained section of postmortem material from the lung of a patient with cystic fibrosis, who died as a result of a chronic infection with . Note that the bacterial cells are embedded in a very large amount of matrix material that has been condensed by dehydration during fixation and preparation.

Citation: William Costerton J. 2004. A Short History of the Development of the Biofilm Concept, p 4-19. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch1
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Image of FIGURE 8
FIGURE 8

TEM of a section of tissue from the area around a surgical staple that had become colonized but not infected by natural skin organisms. Note the extent to which these gram-positive cells occupy the area immediately surrounding the distinctive collagen bundle.

Citation: William Costerton J. 2004. A Short History of the Development of the Biofilm Concept, p 4-19. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch1
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Image of FIGURE 9
FIGURE 9

Diagrammatic representation of the structure of a typical biofilm, formed by cells of in single-species flow cells and in natural systems (e.g., alpine streams). The sessile cells are actually enclosed in matrix material, in structures that resemble mushrooms or simple towers, and interspersed between open water channels in which convective flow occurs. These matrix-enclosed microcolonies are viscoelastic, they are deformed in high flow, and they may simply detach from the surface if the shear force exceeds their tensile strength. This structure is typical of many biofilms, but the structure may vary between species and in response to changing environmental conditions. (Reprinted from Potera, 1998, with permission.)

Citation: William Costerton J. 2004. A Short History of the Development of the Biofilm Concept, p 4-19. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch1
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References

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