Abstract
The biosynthetic capabilities of microbes underlie their growth and interactions, playing a prominent role in microbial community structure. For large, diverse microbial communities, prediction of these capabilities is limited by uncertainty about metabolic functions and environmental conditions. To address this challenge, we propose a probabilistic method, inspired by percolation theory, to computationally quantify how robustly a genome-derived metabolic network produces a given set of metabolites under an ensemble of variable environments. We used this method to compile an atlas of predicted biosynthetic capabilities for 97 metabolites across 456 human oral microbes. This atlas captures taxonomically-related trends in biomass composition, and makes it possible to estimate inter-microbial metabolic distances that correlate with microbial co-occurrences. We also found a distinct cluster of fastidious/uncultivated taxa, including several Saccharibacteria (TM7) species, characterized by their abundant metabolic deficiencies. By embracing uncertainty, our approach can be broadly applied to understanding metabolic interactions in complex microbial ecosystems.
Highlights
Metabolism, in addition to enabling growth and homeostasis for individual microbes, contributes to the organization of complex, dynamic microbial communities
We started with the E. coli core metabolic network, a simplified network consisting of central carbon metabolism and lacking peripheral metabolic pathways, such as amino acid or cofactor biosynthesis (Orth et al, 2010b)
Our method provides an estimate of the putative biosynthetic capabilities of a metabolic network from genomic information
Summary
Metabolism, in addition to enabling growth and homeostasis for individual microbes, contributes to the organization of complex, dynamic microbial communities. Through cross-feeding, a compound produced by one species might benefit another, leading to a network of metabolic interdependences (Embree et al, 2015; Goldford et al, 2017; Mee et al, 2014; Pande et al, 2015; D’Souza et al, 2018; Zengler and Zaramela, 2018; Pacheco et al, 2019; Mee and Wang, 2012) This type of interaction has been proposed as one of the main reasons for the prevalence, in natural microbial communities, of uncultivated (or fastidious) microbes (Stewart, 2012; Epstein, 2013; Pande and Kost, 2017; Staley and Konopka, 1985). The prominence of uncultivated/fastidious microbial organisms across the tree of life and their potential importance in microbial community structure is highlighted by the recent identification of the candidate phyla radiation – a large branch of the tree of life consisting mainly of uncultivated organisms with small
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