Role of priority effects in the early-life assembly of the gut microbiota

Key Points

  • Infant gut microbiota assembly is driven by four ecological processes — dispersal, diversification, drift and selection — and can be understood by resolving their relative contributions, mechanisms and interactive effects

  • Priority effects, whereby the order and timing of dispersal alters how diversification, drift and selection affect infant gut microbiota assembly, could have long-lasting consequences for host health

  • Priority effects in the infant gut are influenced by the regional species pool, which is made up of numerous local communities, some of which are host-associated, while others are not

  • To understand the role of priority effects in the infant gut, future studies in model systems should intentionally vary dispersal order and timing

  • In future studies, when intentional variation in dispersal order is not feasible, dispersal order should be carefully recorded along with relevant environmental variables

  • An understanding of the processes that govern priority effects can be used to inform microorganism-based therapies and manage strategies aimed at guiding the microbiota towards a healthy state

Abstract

Understanding how microbial communities develop is essential for predicting and directing their future states. Ecological theory suggests that community development is often influenced by priority effects, in which the order and timing of species arrival determine how species affect one another. Priority effects can have long-lasting consequences, particularly if species arrival history varies during the early stage of community development, but their importance to the human gut microbiota and host health remains largely unknown. Here, we explore how priority effects might influence microbial communities in the gastrointestinal tract during early childhood and how the strength of priority effects can be estimated from the composition of the microbial species pool. We also discuss factors that alter microbial transmission, such as delivery mode, diet and parenting behaviours such as breastfeeding, which can influence the likelihood of priority effects. An improved knowledge of priority effects has the potential to inform microorganism-based therapies, such as prebiotics and probiotics, which are aimed at guiding the microbiota towards a healthy state.

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Figure 1: Four processes that affect ecological communities.
Figure 2: Contrasting hypothetical patterns of community assembly in the infant gut.
Figure 3: Hypotheses on species features causing strong priority effects.
Figure 4: Local species pools that contribute to the regional pool of microorganisms available for colonization of the infant gut.

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Acknowledgements

The authors' work is supported by the US National Science Foundation (NSF) Graduate Research Fellowship award number DGE-114747 (D.S.), the National Institute of General Medical Sciences of the NIH under award number T32GM007276 (D.S.), the Thomas C. and Joan M. Merigan Endowment at Stanford University (D.A.R.), The Leona and Harry B. Helmsley Foundation grant number 2014PG-IBD014 (D.A.R.), US NSF award numbers DEB-1555786 and DEB-1737758 (T.F.) and the Terman Fellowship of Stanford University (T.F.). Any opinion, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the US NSF or the NIH. The authors especially thank E. Costello for her helpful feedback.

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All authors researched data for the article and provided substantial contributions to discussion of the content. D.S. wrote the article. All authors contributed equally to reviewing and/or editing of the manuscript before submission.

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Correspondence to David A. Relman.

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PowerPoint slides

Glossary

Community assembly

The construction and maintenance of local communities through sequential, repeated immigration of species from a regional species pool.

Regional species pool

The set of species that could potentially colonize and establish within a community.

Niche pre-emption

Occurs when the first species to arrive in a given habitat uses or otherwise sequesters resources and, as a consequence, inhibits the colonization of later species.

Community state types

(CSTs). Categories of stereotypical microbial communities that are typically defined by their dominant taxa and found at a given body site.

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Sprockett, D., Fukami, T. & Relman, D. Role of priority effects in the early-life assembly of the gut microbiota. Nat Rev Gastroenterol Hepatol 15, 197–205 (2018). https://doi.org/10.1038/nrgastro.2017.173

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