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The ecological roles of bacterial chemotaxis

Nature Reviews Microbiology volume 20, pages 491–504 (2022)Cite this article

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A Publisher Correction to this article was published on 01 April 2022

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Abstract

How bacterial chemotaxis is performed is much better understood than why. Traditionally, chemotaxis has been understood as a foraging strategy by which bacteria enhance their uptake of nutrients and energy, yet it has remained puzzling why certain less nutritious compounds are strong chemoattractants and vice versa. Recently, we have gained increased understanding of alternative ecological roles of chemotaxis, such as navigational guidance in colony expansion, localization of hosts or symbiotic partners and contribution to microbial diversity by the generation of spatial segregation in bacterial communities. Although bacterial chemotaxis has been observed in a wide range of environmental settings, insights into the phenomenon are mostly based on laboratory studies of model organisms. In this Review, we highlight how observing individual and collective migratory behaviour of bacteria in different settings informs the quantification of trade-offs, including between chemotaxis and growth. We argue that systematically mapping when and where bacteria are motile, in particular by transgenerational bacterial tracking in dynamic environments and in situ approaches from guts to oceans, will open the door to understanding the rich interplay between metabolism and growth and the contribution of chemotaxis to microbial life.

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Fig. 1: Chemotactic bacterial motility across different environments.
Fig. 2: Relative cost of bacterial chemotaxis depends on the metabolic state of a cell.
Fig. 3: Importance of chemotaxis in individual and collective motility.
Fig. 4: Motility and chemotaxis can drive community diversity.

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Acknowledgements

The authors thank all cited authors for the work highlighted in this Review and apologize to those not cited for length reasons. They are grateful to U. Alcolombri, Z. Landry, J. Nguyen, C. Martinez-Pérez and J. Wheeler for critical reading of the manuscript, and to V. Fernandez, N. Norris and U. Sauer for stimulating discussions. They thank R. Naisbit for scientific editing. The authors were supported by the Simons Foundation through the Principles of Microbial Ecosystems (PriME) collaboration (grant 542395) and the Swiss National Science Foundation’s National Centre of Competence in Research (NCCR) Microbiomes (no. 51NF40_180575 to R.S.).

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  1. These authors contributed equally: Johannes M. Keegstra, Francesco Carrara.

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  1. Institute for Environmental Engineering, ETH Zurich, Zurich, Switzerland

    Johannes M. Keegstra, Francesco Carrara & Roman Stocker

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Contributions

J.M.K. and F.C. researched data for the article. All authors contributed to the discussion of the content, wrote the article and reviewed and edited the manuscript before submission.

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Correspondence to Johannes M. Keegstra or Roman Stocker.

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Nature Reviews Microbiology and the authors acknowledge Terence Hwa and the other, anonymous, reviewers for their contribution to the peer review of this work.

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Dedication

We dedicate this work to the memory of Howard C. Berg (1934–2021), a true giant in illuminating the microscale world of microorganisms, who unravelled the mechanisms of bacterial sensing and locomotion to an unprecedented level. His creative insights have represented the foundation for countless chemotaxis studies over the past decades and will remain an inspiration for future discoveries in the motile lives of bacteria.

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Glossary

Flagella

Elongated, thin and stiff filaments that generate forward thrust by rotating. Multiple filaments together may form a flagellar bundle.

Random walk

Movement in which steps are taken in random directions. It can be biased if the step length or orientation favours a certain direction.

Chemoattractants

Chemicals that attract an organism, inducing movement towards higher concentrations of the chemical.

Metabolism

The chemical reactions required to sustain living systems: breakdown of chemicals to release energy (catabolism), synthesis of biomass (anabolism) and elimination of waste chemicals.

Chemorepellents

Chemicals that repel an organism, inducing movement towards lower concentrations of the chemical.

Flagellar motor

A transmembrane protein complex connecting to the flagellar filaments, which converts a protonic or ionic gradient into rotary motion.

Sensory adaptation

The (partial) restoration of pre-stimulus behaviour during prolonged stimulation.

Chemoreceptors

Elongated transmembrane proteins in which binding to a ligand molecule induces a conformational change that affects downstream pathway activity.

Trade-off

A situation in which a certain trait cannot increase without a decrease in another trait because of certain physical or biological constraints. When the constraint is lifted, the trade-off disappears.

Adaptation time

The time required for the pathway activity and tumble bias to restore to pre-stimulus levels after prolonged stimulation.

Phenotypic diversity

The variation in the biological traits among members of an isogenic population due to biochemical noise.

Tumble bias

The relative proportion of time that a bacterium spends reorienting during motility. Cells with high tumble bias reorient more frequently.

Pathway gain

How strongly a cell amplifies the signal from a given chemical gradient. The amplification is determined by the properties of the signal transduction machinery.

Effective diffusivity

The rate at which a randomly swimming cell explores space.

Brownian random walk

A type of random walk of small particles in a fluid, driven by thermal effects, which results in diffusive behaviour.

Lévy flight

A type of superdiffusive random walk in which the step-length distribution is heavy tailed, leading to increased spatial exploration compared with Brownian motion.

Allee effect

A positive density dependence of individual fitness which arises from cooperation or facilitation among individuals in the population.

Glycolytic

Using the glycolysis pathway to generate energy.

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Keegstra, J.M., Carrara, F. & Stocker, R. The ecological roles of bacterial chemotaxis. Nat Rev Microbiol 20, 491–504 (2022). https://doi.org/10.1038/s41579-022-00709-w

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