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The role of microbial motility and chemotaxis in symbiosis

Abstract

Many symbiotic relationships rely on the acquisition of microbial partners from the environment. However, the mechanisms by which microbial symbionts find and colonize their hosts are often unknown. We propose that the acquisition of environmental symbionts often necessitates active migration and colonization by the symbionts through motility and chemotaxis. The pivotal role of these behaviours in the onset and maintenance of symbiotic interactions is well established in a small number of model systems but remains largely overlooked for the many symbioses that involve the recruitment of microbial partners from the environment. In this Review, we highlight when, where and how chemotaxis and motility can enable symbiont recruitment and propose that these symbiont behaviours are important across a wide range of hosts and environments.

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Fig. 1: Motility-mediated and chemotaxis-mediated symbioses in different habitats.
Fig. 2: Motility of symbionts.
Fig. 3: The opportunity for chemotaxis depending on host size.

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Acknowledgements

This research was funded in part by the Gordon and Betty Moore Foundation Marine Microbiology Initiative, through grant GBMF3801 to J.R.S. and R.S. and an Investigator Award (GBMF3783) to R.S., as well as through an Australian Research Council grant (DP180100838) to J.R.S. and J.-B.R., an Australian Research Council Fellowship (DE160100636) to J.-B.R. and a grant from the Simons Foundation (542395) to R.S. as part of the Principles of Microbial Ecosystems (PriME) Collaborative.

Author contributions

V.F., B.L. and J.-B.R. researched data for the article. V.F. carried out the theoretical component of this work. All authors contributed substantially to discussion of the content, wrote the article and reviewed and edited the manuscript before submission.

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Nature Reviews Microbiology thanks Y. Kikuchi, M. Mandel and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Glossary

Chemotaxis

The ability of microorganisms to sense chemical gradients and direct their movement either up the gradient towards the source (attraction) or down the gradient away from the source (repulsion).

Flagella

Filamentous extracellular appendages that are responsible for the active movement of cells in a liquid environment. Beyond cell motility, flagella are also involved in a range of processes including adhesion, secretion of compounds, virulence and differentiation into biofilms.

Brownian motion

Continuous movement of micrometre-scale particles and organisms in liquid driven by random collisions with water molecules.

Rhizosphere

The zone immediately surrounding the roots of a plant that is enriched in molecules secreted from the root into the soil, providing a key interface for the ecological relationships and chemical exchanges between plants and soil microorganisms.

Diffusion

The spread of dissolved compounds from an area of high concentration to an area of lower concentration, driven by random fluctuations. This rate is set by the diffusivity (D) of the compound, and the spread of a diffusing cloud progressively slows down as it grows in size.

Viscous boundary layer

The region of fluid in the immediate vicinity of a surface where the effects of viscosity are substantial. Fluid flow decreases with proximity to the surface.

Diffusion boundary layer

A region of fluid near a surface where transport of dissolved compounds is dominated by diffusion rather than advection by flow. The size of this region depends on the diffusivity of the compounds and the viscous boundary layer.

Turbulence

A common type of stochastic, chaotic flow composed of interacting vortices across a range of scales.

Shear flows

A type of flow in which the fluid moves in parallel directions but with changing magnitude. Shear flow exists in regions with gradients in velocity, such as the region between a surface with no flow and a constant external flow parallel to the surface.

Feeding currents

Fluid motion generated by an organism to increase prey encounter. These currents can be generated through beating cilia (in protists), mouth appendages (in copepods) or specialized ciliated cells (in sponges).

Pili

Thin filamentous appendages made out of extracellular protein fibres that are involved in various microbial behaviours, including attachment, twitching motility and virulence.

Mucus

Viscous aqueous secretion typically produced by specialized cells that has a role in the protection against infectious agents. Mucus coats the gastrointestinal, respiratory and urogenital tracts of most animals, as well as the external surfaces of marine organisms.

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Raina, JB., Fernandez, V., Lambert, B. et al. The role of microbial motility and chemotaxis in symbiosis. Nat Rev Microbiol 17, 284–294 (2019). https://doi.org/10.1038/s41579-019-0182-9

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