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Priority effects in microbiome assembly

An Author Correction to this article was published on 01 October 2021

This article has been updated

Abstract

Advances in next-generation sequencing have enabled the widespread measurement of microbiome composition across systems and over the course of microbiome assembly. Despite substantial progress in understanding the deterministic drivers of community composition, the role of historical contingency remains poorly understood. The establishment of new species in a community can depend on the order and/or timing of their arrival, a phenomenon known as a priority effect. Here, we review the mechanisms of priority effects and evidence for their importance in microbial communities inhabiting a range of environments, including the mammalian gut, the plant phyllosphere and rhizosphere, soil, freshwaters and oceans. We describe approaches for the direct testing and prediction of priority effects in complex microbial communities and illustrate these with re-analysis of publicly available plant and animal microbiome datasets. Finally, we discuss the shared principles that emerge across study systems, focusing on eco-evolutionary dynamics and the importance of scale. Overall, we argue that predicting when and how current community state impacts the success of newly arriving microbial taxa is crucial for the management of microbiomes to sustain ecological function and host health. We conclude by discussing outstanding conceptual and practical challenges that are faced when measuring priority effects in microbiomes.

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Fig. 1: Priority effects between macroorganisms and between members of their microbiomes in a hypothetical terrestrial ecosystem.
Fig. 2: Examples of priority effects with varying impacts on function.
Fig. 3: Approaches for detecting candidate priority effects in time-series microbiome data.
Fig. 4: Identifying strains of interest in destructively sampled microbiome data.
Fig. 5: Priority effects act on a range of spatial and temporal scales.

Change history

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Acknowledgements

R.D. was supported by the National Science Foundation Graduate Research Fellowship (grant no. 1650114). The authors thank members of the graduate seminar ‘Microbiomes in and as Food Webs’ for helpful discussion.

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R.D., R.A.H., A.L.J. and A.C.-C. researched data for the article and wrote the article. All authors contributed substantially to discussion of the content and reviewed and edited the manuscript before submission.

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Correspondence to Reena Debray or Robin A. Herbert.

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Glossary

Priority effects

Refers, in the narrowest sense, to instances in which the outcomes of species interactions vary according to the order of arrival but is often broadened (including here) to include instances in which arrival timing and/or the abundances of resident species affect the ability of new species to establish.

Perturbation

A change in the biotic or abiotic environment that affects organisms in an ecological community; considered a pulse perturbation (or disturbance) when it is brief compared with the population timescales of relevant organisms or a press perturbation (stress, regime shift) if it is more prolonged.

Trophic resources

Any resource that can be metabolized for biomass production.

Non-trophic resources

Any resource that aids the growth or survival of an organism without being consumed for biomass or energy.

Exploitative competition

An adverse indirect interaction between consumers caused by depleting a shared limiting resource.

Interference competition

An adverse direct interaction between species, generally mediated by harmful behaviours or chemicals.

Apparent competition

An adverse indirect interaction between species that increases the abundance or impact of a common enemy (pathogen, consumer, antibody or predator).

Keystone taxa

A species or strain whose effect is large and disproportionate to its abundance in a community.

Metacommunity

A set of interacting communities that are linked by dispersal.

Community coalescence

The mixing of multiple ecological communities.

Ecological character displacement

Evolutionary divergence of species with overlapping ranges to lessen resource competition.

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Debray, R., Herbert, R.A., Jaffe, A.L. et al. Priority effects in microbiome assembly. Nat Rev Microbiol (2021). https://doi.org/10.1038/s41579-021-00604-w

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