Abstract

Microorganisms modify their environment by excreting by-products of metabolism, which can create new ecological niches that can help microbial populations diversify. A striking example comes from experimental evolution of genetically identical Escherichia coli populations that are grown in a homogeneous environment with the single carbon source glucose. In such experiments, stable communities of genetically diverse cross-feeding E. coli cells readily emerge. Some cells that consume the primary carbon source glucose excrete a secondary carbon source, such as acetate, that sustains other community members. Few such cross-feeding polymorphisms are known experimentally, because they are difficult to screen for. We studied the potential of bacterial metabolism to create new ecological niches based on cross-feeding. To do so, we used genome scale models of the metabolism of E. coli and metabolisms of similar complexity, to identify unique pairs of primary and secondary carbon sources in these metabolisms. We then combined dynamic flux balance analysis with analytical calculations to identify which pair of carbon sources can sustain a polymorphic cross-feeding community. We identified almost 10,000 such pairs of carbon sources, each of them corresponding to a unique ecological niche. Bacterial metabolism shows an immense potential for the construction of new ecological niches through cross feeding.

Highlights

  • With as many as one trillion predicted species, microbial diversity on our planet is enormous [1]

  • Biodiversity can emerge in a completely homogeneous environment from populations with initially genetically identical individuals. This striking observation comes from experimental evolution of bacteria, which create new ecological niches when they excrete nutrient-rich waste products that can sustain the life of other bacteria

  • We used experimentally validated models of bacterial metabolism to predict how many novel niches organisms like Escherichia coli can construct, if a novel niche must be able to sustain a stable community of microbes that differ in the nutrients they consume

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Summary

Introduction

With as many as one trillion predicted species, microbial diversity on our planet is enormous [1]. To understand the origins of biological diversity in general and microbial diversity in particular is a central goal of ecology and evolutionary biology. Most biological diversity was thought to arise in allopatry, that is, when populations become physically subdivided [2]. Biologists have increasingly accepted that populations can diversify in sympatry, that is, without any physical barriers [3,4,5,6,7,8,9]. Examples of sympatric diversification include insect populations that adapt evolutionarily to different plant hosts [9], stickleback populations that evolve reproductive isolation at least partly in sympatry [6], Midas cichlid populations that originated in a small volcanic crater lake in Nicaragua [7], and bacteriophage lambda that specializes on different bacterial hosts [8]. Sympatric divergence has been observed both in nature [10,11] and during experimental evolution [12,13,14,15]

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