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

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.

Figure 1 |. Four processes that affect ecological communities.

a | The arrow represents dispersal of an organism (orange circle) from Environment 1 (orange shading) to Environment 2 (blue shading). b | Deterministic fitness differences between two species (orange circle, blue triangle) cause the orange environment to select for one (orange circle) and against the other (blue triangle). c | Stochastic changes in the relative abundances of two species (orange area and blue area) result in changes in community structure within one environment through time. As a result, one population (blue) has gone locally extinct by the end of the time period. d | Mutation and/or recombination within a population (blue and orange areas) results in new genetic variation through time, leading to new strains (as denoted by different shades).

Figure 2 |. Contrasting hypothetical patterns of community assembly in the infant gut.

An illustration of how infant microbial communities assemble with deterministic host selection (top) or priority effects (bottom). The shapes represent different taxa, while the colours represent the community state. Under deterministic host selection, the state of the assembling community is determined by host features that select for the blue microorganisms regardless of colonization order. With priority effects, colonization order can matter more than species identity.

Figure 3 |. Hypotheses on species features causing strong priority effects.

Both early-colonizing (Microorganism 1) and late-colonizing (Microorganism 2) microorganisms have their own set of requirements for colonizing a given environment as well as a distinct effect on that environment. The width of the arrow denotes the strength of each microorganism’s effect niche and requirement niche. a | Microorganism 1 has a large effect on its environment, resulting in a modified niche that inhibits colonization by Microorganism 2. b | Microorganism 2 has a high niche requirement and is therefore more sensitive to smaller modifications to the niche that can inhibit its colonization. c | Microorganisms 1 and 2 have high niche overlap, meaning that Microorganism 1 is able to pre-empt the niche and inhibit colonization by Microorganism 2. Niche overlap is not necessary if the priority effects occur by way of the environment, as in parts a and b.

Figure 4 |. Local species pools that contribute to the regional pool of microorganisms available for colonization of the infant gut.

Infants are colonized by microorganisms from host-associated communities, environmental communities that are not host adapted, and unknown microbial sources. The thickness of the arrows denotes the hypothesized relative contributions of microorganisms from different sources that disperse to and stably colonize the local community (infant gastrointestinal tract).