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The biofilm life cycle: expanding the conceptual model of biofilm formation

Abstract

Bacterial biofilms are often defined as communities of surface-attached bacteria and are typically depicted with a classic mushroom-shaped structure characteristic of Pseudomonas aeruginosa. However, it has become evident that this is not how all biofilms develop, especially in vivo, in clinical and industrial settings, and in the environment, where biofilms often are observed as non-surface-attached aggregates. In this Review, we describe the origin of the current five-step biofilm development model and why it fails to capture many aspects of bacterial biofilm physiology. We aim to present a simplistic developmental model for biofilm formation that is flexible enough to include all the diverse scenarios and microenvironments where biofilms are formed. With this new expanded, inclusive model, we hereby introduce a common platform for developing an understanding of biofilms and anti-biofilm strategies that can be tailored to the microenvironment under investigation.

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Fig. 1: The original five-step model of biofilm development.
Fig. 2: Variation in Pseudomonas aeruginosa biofilm architecture.
Fig. 3: Diverse surface-attached and non-surface-attached biofilm structures.
Fig. 4: Mechanisms of microbial aggregate formation.
Fig. 5: Expanded conceptual model of biofilm formation.

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Acknowledgements

The authors thank J. Story for help with preparing Fig. 3.

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Glossary

Aggregates

Cohesive groups of microbial cells surrounded by extracellular polymeric substances and other entrapped abiotic or biotic materials. Microbial aggregates can be surface attached, matrix associated or free floating in the liquid phase and display a biofilm-like phenotype.

Biofilms

Microbial aggregates attached or associated with a surface and embedded in a matrix. These can include single or multiple discrete aggregates or more continuous films.

Aggregation

Any biological, chemical or physical process that enables microbial cells to form an aggregate.

Growth

Expansion of aggregates by microbial growth and concomitant production of extracellular polymeric substance, whether in suspension or attached to a surface.

Attachment

Suspended single cells or aggregates adhere to a host cellular surface or an abiotic surface, either directly to the substratum or to previously attached microbial cells or clusters.

Detachment

An overarching term encompassing all phase transfer processes in which microbial cells and extracellular polymeric substances move from the surface-attached phase to a fluid-borne phase. This term is specific to surface-attached biofilms.

Dispersal

Specifically connotes an active and biologically regulated release of microbial cells from a suspended or attached biofilm aggregate.

Disaggregation

Aggregated cells, whether in suspension or associated with a surface, that shed smaller microbial aggregates or individual cells into the fluid phase.

Accumulation

The net result of attachment, aggregation, growth, disaggregation and detachment processes that leads to expansion or shrinkage of a biofilm or aggregate.

Removal

Implies the response to a mechanical, chemical or enzymatic intervention that causes attached aggregates or cells to be released from the surface.

Polymer bridging

The aggregation of microbial cells in suspension caused by polymers that adhere to cell wall components forming bridging bonds between multiple cells.

Sloughing

The release of coherent layers of surface-attached biofilm by adhesive failure (that is, at the biofilm–substratum interface), generally by fluid shear. This mechanism is specific to surface-attached biofilms.

Co-aggregation

The formation of aggregates (also known as clumps) in suspension by bacteria of different species.

Depletion aggregation

The formation of aggregates in suspension through a colloidal physics phenomenon that occurs when polymers in solution are of high enough concentration and molecular weight to initiate phase separation, ‘forcing’ microbial cells together.

Auto-aggregation

The formation of aggregates (also known as clumps) in suspension by bacteria of the same species.

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Sauer, K., Stoodley, P., Goeres, D.M. et al. The biofilm life cycle: expanding the conceptual model of biofilm formation. Nat Rev Microbiol 20, 608–620 (2022). https://doi.org/10.1038/s41579-022-00767-0

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