Abstract

The human gut microbiome is a complex ecosystem, in which hundreds of microbial species and metabolites coexist, in part due to an extensive network of cross-feeding interactions. However, both the large-scale trophic organization of this ecosystem, and its effects on the underlying metabolic flow, remain unexplored. Here, using a simplified model, we provide quantitative support for a multi-level trophic organization of the human gut microbiome, where microbes consume and secrete metabolites in multiple iterative steps. Using a manually-curated set of metabolic interactions between microbes, our model suggests about four trophic levels, each characterized by a high level-to-level metabolic transfer of byproducts. It also quantitatively predicts the typical metabolic environment of the gut (fecal metabolome) in approximate agreement with the real data. To understand the consequences of this trophic organization, we quantify the metabolic flow and biomass distribution, and explore patterns of microbial and metabolic diversity in different levels. The hierarchical trophic organization suggested by our model can help mechanistically establish causal links between the abundances of microbes and metabolites in the human gut.

Author summary

Trillions of microbial inhabitants of a human gut play a crucial role in human health and disease. This ecosystem is composed of hundreds of individual species and shaped by extensive nutrient exchange. The network of such cross-feeding interactions between microbes has been extensively studied and shown to be staggeringly complex. Here we propose an algorithm to arrange this network in multiple trophic levels guiding the flow of nutrients from lower to higher levels. This organization is reminiscent of macroscopic food webs converting the biomass from plants to herbivores and ultimately to carnivore predators. We build a simplified model, providing quantitative support for a multi-level organization of the human gut microbiome. It allows us to predict the typical metabolic environment of the gut (fecal metabolome) in individual patients that is in approximate agreement with the experimental data. The hierarchical trophic organization suggested by our model can help establish causal links between the abundances of microbes and metabolites in the human gut.

Credit: CC0 Public Domain

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Citation: Wang T, Goyal A, Dubinkina V, Maslov S (2019) Evidence for a multi-level trophic organization of the human gut microbiome. PLoS Comput Biol 15(12): e1007524. https://doi.org/10.1371/journal.pcbi.1007524

Photo credit:  G.steph.rocket [CC BY-SA 4.0 (https://creativecommons.org/licenses/by-sa/4.0)], from Wikimedia Commons