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Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal

Key Points

  • The predominant mode of growth of most bacteria in natural and engineered environments is as a surface-associated community encased in an extracellular matrix, called a biofilm. When conditions within the biofilm become unfavourable, bacteria must be able to disperse to escape and colonize new habitats.

  • The dispersal response of bacterial biofilms is regulated through the production and perception of extracellular and intracellular signalling molecules and in response to environmental cues such as changes in nutrient concentrations. Such signals and cues are translated into changes in gene expression that induce effectors, such as enzymes and surfactants, which break down the biofilm matrix and prepare bacteria for planktonic growth.

  • In addition to releasing bacteria to colonize new sites, dispersal is associated with the formation of genetic variants that may be altered in traits which are important for colonization of and competition in new habitats.

  • The sessile (biofilm) and motile (dispersal) phases of bacterial growth have close analogies to the lifestyles of colonial and holometabolous eukaryotes, including the generation of variants in the dispersal propagules. Biofilms may therefore be useful experimental tools to further explore ecological and evolutionary theories surrounding organisms with sessile and motile life phases.

Abstract

In most environments, bacteria reside primarily in biofilms, which are social consortia of cells that are embedded in an extracellular matrix and undergo developmental programmes resulting in a predictable biofilm 'life cycle'. Recent research on many different bacterial species has now shown that the final stage in this life cycle includes the production and release of differentiated dispersal cells. The formation of these cells and their eventual dispersal is initiated through diverse and remarkably sophisticated mechanisms, suggesting that there are strong evolutionary pressures for dispersal from an otherwise largely sessile biofilm. The evolutionary aspect of biofilm dispersal is now being explored through the integration of molecular microbiology with eukaryotic ecological and evolutionary theory, which provides a broad conceptual framework for the diversity of specific mechanisms underlying biofilm dispersal. Here, we review recent progress in this emerging field and suggest that the merging of detailed molecular mechanisms with ecological theory will significantly advance our understanding of biofilm biology and ecology.

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Figure 1: The complex structure of bacterial biofilms.
Figure 2: Active biofilm dispersal and variant formation.

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Acknowledgements

The authors acknowledge S. Longford for help with the figures and the Australian Research Council, Environmental Biotechnology Cooperative Research Centre and National Health and Medical Research Council for ongoing and long term support of this research. This is publication number 0058 of the Sydney Institute of Marine Science, Australia.

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Correspondence to Staffan Kjelleberg.

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Glossary

Dispersal

The movement of an individual organism away from the parent organism or population to a new niche.

Cell communication signals

Molecules that are produced and perceived by an organism. Signals are produced at a particular stage of growth under specific conditions or in response to changes in the environment. They accumulate extracellularly and are recognized by a dedicated receptor to induce a concerted response when a critical threshold has been reached. To be classed as cell communication, this response must extend beyond that which is required for metabolism or detoxification of the substance.

Second messenger

An intracellular molecule (usually small and rapidly diffusible) that transmits information from a receptor to a target molecule; for example, cyclic AMP and cyclic di-GMP.

Chemotaxis

The movement of cells or organisms according to chemical concentration gradients in the environment, either towards or away from the stimulus.

Nitric oxide

(NO). A small, reactive gas and a universal signalling molecule in biological systems (as initially discovered in the 1970s, for its role in regulating vasodilation in mammals). In bacteria, NO is generated as a by-product of anaerobic metabolism or by NO synthases (NOSs).

Autoinducing peptides

Extracellular peptides, ranging from 5 to 34 amino acids in length, that are generated by cleavage from precursor peptides and then further post-transcriptionally modified. These peptides are used by Gram-positive bacteria as cell communication signals.

Sensor regulator

A protein that receives and responds to information about changes in the environment, either by binding second messengers or through phosphorylation, to induce transcriptional changes.

Response regulator

The phosphorylation-dependent modulator of a two-component phosphorelay system. The partner sensor protein responds to environmental stimuli to modulate the phosphorylation status of the regulator, and the resultant phosphorylation cascade drives the response through differential expression of target genes.

Lysogenic

Pertaining to a bacteriophage genome: being incorporated into the chromosome of the host bacterium, resulting in transmission to daughter bacterial cells on cell division. Lysogenic phages are referred to as prophages.

Bet hedging

An evolutionary response to variable environments. In the context of dispersal, it is predicted to manifest in a number of ways, including the production of different types of dispersal cells to maximize colonization of different habitats, and spreading dispersal in time to accommodate temporally varying habitats.

Colonial

Of an organism: able to form replicate, more or less identical units ('modules') via asexual means; these units then often connect physically and physiologically to form a colony. Monospecies biofilms are colonial (or modular, or clonal) in this sense.

Holometabolous

Pertaining to an insect: with a life cycle in which there is a larval phase that is morphologically and ecologically distinct from the adult phase and which must undergo 'complete metamorphosis' via a pupal phase before becoming an adult. Examples include butterflies and true flies.

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McDougald, D., Rice, S., Barraud, N. et al. Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nat Rev Microbiol 10, 39–50 (2012). https://doi.org/10.1038/nrmicro2695

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