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

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  • Román Zapién-Campos
  • Michael Sieber
  • Arne Traulsen

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.Author summary: Microbial communities are prevalent not only in the environment but also in hosts. Although the drivers of environmental microbiomes have been studied extensively, less is known about the drivers distinguishing a host environment. Recent experimental observations have highlighted the influence of ecological drift in hosts with short lifespan, including model organisms like C. elegans, D. melanogaster and D. rerio. We have developed a theoretical model to study the effect of a finite host lifespan on relevant observables of the microbiome, including the microbial load, probability of colonization of a microbial taxon, and distribution of microbiome composition in a host population. Although we focus on a case free of any selection, our results indicate the possible coexistence of hosts with alternative microbiome composition, and to a larger extent the coexistence of colonized and microbe-free hosts. A quantitative description is provided.

Suggested Citation

  • Román Zapién-Campos & Michael Sieber & Arne Traulsen, 2020. "Stochastic colonization of hosts with a finite lifespan can drive individual host microbes out of equilibrium," PLOS Computational Biology, Public Library of Science, vol. 16(11), pages 1-20, November.
  • Handle: RePEc:plo:pcbi00:1008392
    DOI: 10.1371/journal.pcbi.1008392
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    References listed on IDEAS

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    1. Kyriakidis, E. G., 1994. "Stationary probabilities for a simple immigration-birth-death process under the influence of total catastrophes," Statistics & Probability Letters, Elsevier, vol. 20(3), pages 239-240, June.
    2. Randall J. Swift, 2001. "Transient probabilities for a simple birth-death-immigration process under the influence of total catastrophes," International Journal of Mathematics and Mathematical Sciences, Hindawi, vol. 25, pages 1-4, January.
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