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Gradients and consequences of heterogeneity in biofilms

Abstract

Historically, appreciation for the roles of resource gradients in biology has fluctuated inversely to the popularity of genetic mechanisms. Nevertheless, in microbiology specifically, widespread recognition of the multicellular lifestyle has recently brought new emphasis to the importance of resource gradients. Most microorganisms grow in assemblages such as biofilms or spatially constrained communities with gradients that influence, and are influenced by, metabolism. In this Review, we discuss examples of gradient formation and physiological differentiation in microbial assemblages growing in diverse settings. We highlight consequences of physiological heterogeneity in microbial assemblages, including division of labour and increased resistance to stress. Our impressions of microbial behaviour in various ecosystems are not complete without complementary maps of the chemical and physical geographies that influence cellular activities. A holistic view, incorporating these geographies and the genetically encoded functions that operate within them, will be essential for understanding microbial assemblages in their many roles and potential applications.

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Fig. 1: O2 gradients influence metabolic differentiation and morphogenesis in multicellular systems.
Fig. 2: Physiological stratification of microbial assemblages along chemical gradients.
Fig. 3: Redox balancing strategies in Pseudomonas aeruginosa biofilms.
Fig. 4: Interplay between resource gradients and biofilm architecture in Pseudomonas aeruginosa and Escherichia coli.
Fig. 5: Gradient formation and examples of metabolite exchange in cyanobacterial mats.
Fig. 6: Physiological heterogeneity enhances overall robustness of microbial assemblages.

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Acknowledgements

Work in the Dietrich laboratory is supported by National Institutes of Health (NIH)/National Institute of Allergy and Infectious Diseases (NIAID) grant R01AI103369.

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Correspondence to Lars E. P. Dietrich.

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Glossary

Communities

Interacting assemblages of multiple species in a common location.

Biofilms

Assemblages of microbial cells encased in a self-produced matrix.

Matrix

An adhesive, extracellular material composed of polysaccharides, DNA and/or proteins produced by microbial cells in biofilms.

Cross-feeding

The exchange of metabolites between cells.

Oxygenic phototrophs

Organisms that use light as a source of energy and water as an electron donor, thereby producing molecular O2.

Morphogen

A signalling molecule that forms a concentration gradient across a developing organism and elicits concentration-dependent responses.

Denitrification

The stepwise reduction of nitrate to nitrogen gas, carried out by integral membrane and membrane-associated proteins. Some steps in denitrification pathways contribute to the proton motive force, and thereby the synthesis of ATP.

Phenazines

Redox-active compounds produced by Pseudomonas aeruginosa and other bacteria that can shuttle electrons between cells and distant oxidants.

Chemotrophic

Using an organic or inorganic chemical (as opposed to light) as a source of energy for metabolism.

Heterotrophs

Organisms that use an organic carbon source in metabolism.

Intertidal mats

Biofilm communities dominated by cyanobacteria that form within the tidal range on seashores.

Autotrophic

Using an inorganic carbon source in metabolism.

Resistance

A (usually heritable) trait conferred, for example, by dedicated proteins that efflux or degrade an antimicrobial compound, allowing the producing organism to grow at antimicrobial concentrations that would otherwise inhibit growth.

Tolerance

A (heritable or non-heritable) trait exhibited by the majority of cells in a population that confers survival during transient exposure to an antimicrobial.

Persistence

A non-heritable property exhibited by a minority of cells in a population that survives exposure to an antimicrobial; that is, tolerance that is restricted to a subpopulation.

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Jo, J., Price-Whelan, A. & Dietrich, L.E.P. Gradients and consequences of heterogeneity in biofilms. Nat Rev Microbiol (2022). https://doi.org/10.1038/s41579-022-00692-2

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