Bacterial adhesion: seen any good biofilms lately?

Abstract

The process of surface adhesion and biofilm development is a survival strategy employed by virtually all bacteria and refined over millions of years. This process is designed to anchor microorganisms in a nutritionally advantageous environment and to permit their escape to greener pastures when essential growth factors have been exhausted. Bacterial attachment to a surface can be divided into several distinct phases, including primary and reversible adhesion, secondary and irreversible adhesion, and biofilm formation. Each of these phases is ultimately controlled by the expression of one or more gene products. Ultrastructurally, the mature bacterial biofilm resembles an underwater coral reef containing pyramidal or mushroom-shaped microcolonies of organisms embedded within an extracellular glycocalyx, with channels and cavities to allow the exchange of nutrients and waste. The biofilm protects its inhabitants from predators, dehydration, biocides, and other environmental extremes while regulating population growth and diversity through primitive cell signals. From a physiological standpoint, surface-bound bacteria behave quite differently from their planktonic counterparts. Recognizing that bacteria naturally occur as surface-bound and often polymicrobic communities, the practice of performing antimicrobial susceptibility tests using pure cultures and in a planktonic growth mode should be questioned. That this model does not reflect conditions found in nature might help explain the difficulties encountered in the management and treatment of biomedical implant infections.

FIG. 1.

Thin-section electron micrographs of exopolysaccharide obtained from a liquid culture of a mucoid strain of Pseudomonas aeruginosa. The micrographs demonstrate individual cells (a and b) and microcolonies (c) entrapped in a matrix of alginic acid exopolysaccharide. Magnification, ×50,000 for panel a and ×30,000 for panels b and c.

FIG. 2.

Scanning electron micrograph of an untreated biofilm of S. epidermidis (a) and an identical biofilm exposed to vancomycin and rifampin for 72 h at concentrations exceeding the MIC and MBC for the organism (b). Despite obvious changes in the treated biofilm, viable organisms were recovered for which the MIC and MBC of both agents were unaltered. Reprinted from reference 31 with permission of the American Society for Microbiology.

FIG. 3.

Schematic representation of biofilm formation by S. epidermidis. Primary adhesion (step 1) of individual cells to a surface is influenced by physical interactions (hydrophobic, electrostatic), which in turn might be influenced by cell surface adhesions. Cellular aggregation (step 2) is mediated by polysaccharide intercellular adhesin (PIA), the gene product of the icaADBC gene cluster, and (speculatively) other factors, such as divalent cations. The final phase (step 3) is characterized by the generation of a slime exopolysaccharide that encases surface-bound organisms in a gelatinous matrix but is not essential to biofilm development.

FIG. 4.

Schematic representation of biofilm formation by P. aeruginosa. Step 1 represents the primary adhesion of individual cells to a targeted surface that is dependent on motility, i.e., the production of functional flagella. The aggregation phase (step 2) of biofilm development requires the synthesis of type IV pili, which allow the cells to migrate across a surface and congregate in microcolonies. The final phase (step 3) of biofilm development by P. aeruginosa calls for the elaboration of an alginic acid-like exopolysaccharide by the algACD gene cluster. Cells near the outer surface can dislodge from the biofilm and escape to colonize new microenvironments.