Stochastic colonization of hosts with a finite lifespan can drive individual host microbes out of equilibrium

Abstract

Macroorganisms are inhabited by microbial communities that often change through the lifespan of an individual. One of the factors contributing to this change is colonization from the environment. The colonization of initially microbe-free hosts is particularly interesting, as their microbiome depends entirely on microbes of external origin. We present a mathematical model of this process with a particular emphasis on the effect of ecological drift and a finite host lifespan. Our results indicate the host lifespan becomes especially relevant for short-living organisms (e.g. Caenorhabditis elegans, Drosophila melanogaster, and Danio rerio). In this case, alternative microbiome states (often called enterotypes), the coexistence of microbe-free and colonized hosts, and a reduced probability of colonization can be observed in our model. These results unify multiple reported observations around colonization and suggest that no selective or deterministic drivers are necessary to explain them.

On the effect of inheritance of microbes in commensal microbiomes

“…(2). In addition to the case without inheritance, which we have previously analyzed elsewhere [28], at least three qualitatively distinct cases may be observed (Fig. 1B), depending on host development, reproduction, and mode of delivery.…”

“…Without microbial inheritance, which will be our reference case throughout, any microbe occurring inside a host has to have migrated from the environment during the host lifespan. As a result, a low environmental migration or short host lifespan can be limiting [28]. The transfer of microbes from parents to offspring during birth could increase the probability of observing any microbes in hosts, P [ x i + o i > 0] inh.…”

“…We observed that the effect of inheritance may differ between taxa. Microbiomes assembled entirely from the environment are prone to variation when migration between hosts is rare [28, 18]. Inheritance might increase the presence of certain microbes, but in contrast to environmental migration, inheritance reduces the variation between hosts and potentially their microbial diversity.…”

“…5). A consistent cargo in seeds might guarantee the presence of certain microbes in plants [17], who might sometimes benefit from being the first colonizers [28]. In contrast, greater variation might be expected for mammals, where changing amounts of microbes are obtained from epithelia during delivery [11, 12].…”

The effect of microbial selection on the occurrence-abundance patterns of microbiomes

“…Although we provided a focused analysis of the occurrence-abundance pattern at equilibrium, future work could study its dynamics [34] and derive exact equations for these and other observables [27]. In addition, identifying neutral and non-neutral types remains an open problem.…”