Abstract

Microorganisms exist almost exclusively in interactive multispecies communities, but genetic determinants of the fitness of interacting bacteria, and accessible adaptive pathways, remain uncharacterized. Here, using a two-species system, we studied the antagonism of Pseudomonas aeruginosa against Escherichia coli. Our unbiased genome-scale approach enabled us to identify multiple factors that explained the entire antagonism observed. We discovered both forms of ecological competition–sequestration of iron led to exploitative competition, while phenazine exposure engendered interference competition. We used laboratory evolution to discover adaptive evolutionary trajectories in our system. In the presence of P. aeruginosa toxins, E. coli populations showed parallel molecular evolution and adaptive convergence at the gene-level. The multiple resistance pathways discovered provide novel insights into mechanisms of toxin entry and activity. Our study reveals the molecular complexity of a simple two-species interaction, an important first-step in the application of systems biology to detailed molecular dissection of interactions within native microbiomes.

Highlights

  • Microorganisms are typically found in complex communities such as those in the soil, aquatic environments, and the microbiome [1], and interactions between microbial species can critically impact their survival and evolutionary trajectories [1, 2]

  • Bacteria commonly exist in nature as part of large multispecies communities, and their behavior is affected by the surrounding species via secreted molecules or physical contact

  • We show that the opportunistic pathogen Pseudomonas aeruginosa inhibits the growth of the commensal Escherichia coli, and we use unbiased genome-scale methods to identify the mediators

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Summary

Introduction

Microorganisms are typically found in complex communities such as those in the soil, aquatic environments, and the microbiome [1], and interactions between microbial species can critically impact their survival and evolutionary trajectories [1, 2]. Current knowledge suggests that competition plays an important role in interspecies microbial interactions [3, 4] This includes both exploitative competition, where species compete for limited nutrients, as well as interference competition, where species directly antagonize each other [5]. Previous studies have identified molecules produced by bacteria that may affect the behavior or fitness of other species. Such molecules could be beneficial to the target species [6], but a wide variety of them have been shown to be antagonistic in nature [7,8,9]. The entire breadth of interactions that determines fitness in a specific multispecies system has rarely been identified and characterized at the molecular level

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