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Science  10 Apr 1998:
Vol. 280, Issue 5361, pp. 226-227
DOI: 10.1126/science.280.5361.226

Communities form by interactions amongst individuals. In the beginning, a few wandering souls find an appropriate location in which to settle. As the population numbers increase at this spot, individuals must communicate closely to ensure adequate distribution of food and removal of wastes. If successful in these early stages, new communities can flourish and stabilize and their members can enjoy the shelter afforded by living in a protective environment.

These words could describe the growth of a village, but the same description can also be applied to community formation by the simplest of all organisms, the bacteria. Despite the widely held view of bacteria as primitive, unicellular organisms that struggle for individual survival, it is becoming clear that bacteria seldom behave as isolated organisms (1). Rather, the apparent simplicity of bacteria belies their extraordinary sophistication in communicating with one another and sometimes with higher organisms as well. Informed by chemical communication, motile cells of the myxobacteria and filamentous cells of the streptomycetes organize themselves into conspicuous multicellular structures that carry out specialized tasks in spore formation and dispersal (2). Furthermore, most bacteria have evolved elaborate mechanisms for adhering to solid surfaces [HN2] and thereby establishing complex communities referred to as biofilms. But it has been mysterious how bacteria in these biofilm communities communicate with each other to coordinate their behavior. In a report appearing on page 295 of this issue, Davies et al. shed new light on cell-to-cell signaling during the development of a bacterial biofilm (3).

Bacterial biofilms are ubiquitous and play a multitude of important roles in different environments. In many instances they provide beneficial effects to other organisms. Such is the case for biofilms of Pseudomonas fluorescens that form on the surface of plant roots, thereby preventing the growth of fungal pathogens. In other situations, bacterial biofilms can have a deadly effect. In a clinical setting biofilms can wreak havoc when they form on catheters or on medical implants. Such infections are extremely difficult to control because biofilm bacteria, for reasons that remain largely unknown, are extremely resistant to the action of antimicrobial agents. [HN3], [HN4]

Even though most microorganisms grow as biofilms and the physical structure of different biofilms is well characterized, until recently, this important life form had not been studied with molecular genetic approaches. This is rapidly changing, and many bacterial mutants are now being analyzed for their effects on biofilm development (3, 4). A good example of the productive results of this approach is the work of Davies et al., who used specific mutants of P. aeruginosa [HN5] to demonstrate that a signal molecule provides a form of cell-to-cell communication that is an essential component for the normal development of biofilms.

The type of molecule responsible for the cell-to-cell communication in P. aeruginosa biofilms—an acylated homoserine lactone (acyl-HSL)—is already familiar to many microbiologists. Acyl-HSLs act as extracellular signaling molecules that control a plethora of phenomena, among them bioluminescence, exoenzyme synthesis, and virulence factor production (5). The acyl-HLSs (as well as many peptides) are secreted by bacteria such that they accumulate in the medium in proportion to the total number of cells. In this way, they provide an index of population densities, earning them the name of quorum sensors. With the new work, it now becomes clear that within a sessile community such signals are critical for the multicellular life of microorganisms.

The formation of biofilms can be considered as a developmental cycle (see the figure). It begins when free-swimming (planktonic) bacteria recognize a surface and firmly attach. For many bacteria, this process requires flagella [HN6], [HN7] or surface adhesins [HN8] and depends on nutritional signals from the environment (4, 6). Subsequently, the attached cells grow and divide and at the same time recruit additional planktonic cells that attach to the cells already on the surface. But left unchecked, simple growth of the bacteria on the surface would eventually lead to extreme crowding, possibly starving many cells that might not be able to obtain nutrients. At the same time, toxic metabolic wastes could accumulate among the densely packed cells. The solution to these problems is to create space between loosely packed clusters of cells. Attached bacteria migrate slightly from the surface as they excrete extracellular polysaccharides that serve as the matrix for the biofilms. As the biofilm architecture develops, cells cluster in pillar- and mushroom-like structures, with water channels between them through which nutrients can flow in and waste products out, functioning very much like a primitive circulatory system (6). Mature biofilms thus have a specialized architecture that ensures the well-being of the individual cells that compose it. The sloughing-off of individual cells from the biofilm completes the developmental cycle.

Construction of a biofilm.

Free (planktonic) bacteria assemble on a surface (left). Cell-to-cell communication then induces the formation of multicellular pillars and columns (right).

Davies et al. have made the important observation that one of two acyl-HSLs synthesized by P. aeruginosa [N-(3-oxododecanoyl)-L-homoserine lactone) is a key signaling molecule in the development of biofilm architecture (3). Mutant cells unable to synthesize this acyl-HSL were still able to initiate biofilm formation by attaching to the surface and multiplying there. But the cells failed to create space between them and failed to form the elaborate architecture of mature biofilms, despite the fact that they produced the same amount of extracellular polysaccharide. Addition of synthetic signal molecule restored the architecture to the biofilm, suggesting that gradients of the molecule per se did not generate the structures characteristic of normal biofilms. Rather, it appears that the presence of the acyl-HSL normally initiates a process of differentiation that eventually leads to the maturation of the biofilm. Clearly, communication amongst cells by extracellular signaling molecules is a key step in the normal development of biofilms.

The work of Davies et al. has only scratched the surface of biofilm development, and these exciting results now open the way for much additional investigation.

HyperNotes Related Resources on the World Wide Web

General Hypernotes

Biofilms Resources is an educational resource developed by the American Society for Microbiology. Biofilms are described and related Web sites are listed.

Biofilms: the Movies is a brief illustrated introduction to biofilms.

Biofilms by Dennis J. O'Melia is an illustrated guide to biofilms covering the formation of biofilms, their role in ecosystems, and biofilms in medicine and industry, and the control of biofilms.

Mathematical Modeling and Visualization of Biofilms and Related Structures presents simulations of biofilm growth.

Medical Microbiology: a Brief Introduction includes a brief description of bacteria.

How Bacteria Swim and Tumble describes bacterial locomotion. This site is presented by Cells Alive!, developed by Quill Graphics and Biology in Motion.

Bacterial Structure outlines the structure of bacteria.

The World Wide Web Virtual Library Biosciences is a comprehensive list of World Wide Web resources for biological sciences.

The American Society for Microbiology provides a list of Web resources for microbiology.

Numbered Hypernotes

1. The Kolter Lab Web page describes the research of Roberto Kolter and his co-workers.

2. Adherence, particularly adherence of pathogenic bacteria to eukaryotic host sites, is outlined in Bacteriology 330 Lecture Topics by Kenneth Todar.

3. In Pseudomonas and the Laboratory Animal, David M. Moore describes the resistance of biofilms to the action of antimicrobial agents.

4. Biofilms, Microbial Ecology and Antoni van Leeuwenhoek presents an introduction to biofilms and describes their resistance to antimicrobial agents.

5. Pseudomonas aeruginosa is described in detail in Bacteriology 330 Lecture Topics by Kenneth Todar.

6. Kingdom Monera: the Prokaryotes provides a general description of bacteria including flagella and bacterial locomotion. This page is a section of the syllabus for Evolution and Biodiversity Laboratory, a course offered at Miami University.

7. What the Heck is a Bacterium's “Tail”? is an informal introduction to bacterial flagella.

8. Bacterial Pathogenesis by A. Maggs outlines the role of adhesins in interactions between pathogenic bacteria and their hosts.

9. Department of Microbiology and Molecular Genetics, Harvard Medical School


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