Siderophore cheating and cheating resistance shape competition for iron in soil and freshwater Pseudomonas communities

Elena Butaitė,Rolf Kümmerli,Stefan Wyder,Michael Baumgartner

doi:10.1038/s41467-017-00509-4

Elena Butaitė, Rolf Kümmerli + Show 2 more

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https://doi.org/10.1038/s41467-017-00509-4

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Journal: Nature Communications	Publication Date: Sep 4, 2017
Citations: 182	License type: open-access

Affiliation: University of Zurich

Abstract

All social organisms experience dilemmas between cooperators performing group-beneficial actions and cheats selfishly exploiting these actions. Although bacteria have become model organisms to study social dilemmas in laboratory systems, we know little about their relevance in natural communities. Here, we show that social interactions mediated by a single shareable compound necessary for growth (the iron-scavenging pyoverdine) have important consequences for competitive dynamics in soil and pond communities of Pseudomonas bacteria. We find that pyoverdine non- and low-producers co-occur in many natural communities. While non-producers have genes coding for multiple pyoverdine receptors and are able to exploit compatible heterologous pyoverdines from other community members, producers differ in the pyoverdine types they secrete, offering protection against exploitation from non-producers with incompatible receptors. Our findings indicate that there is both selection for cheating and cheating resistance, which could drive antagonistic co-evolution and diversification in natural bacterial communities.

Highlights

All social organisms experience dilemmas between cooperators performing group-beneficial actions and cheats selfishly exploiting these actions
While non-producers have genes coding for multiple pyoverdine receptors and are able to exploit compatible heterologous pyoverdines from other community members, producers differ in the pyoverdine types they secrete, offering protection against exploitation from non-producers with incompatible receptors
Social interactions and cheating seem to cover all aspects of microbial life, their role in natural microbial communities remains largely unclear[44,45,46,47]. Our study tackled this gap in knowledge and shows that social interactions mediated by shareable iron-scavenging pyoverdines can have important consequences for strain–to–strain interactions in phylogenetically diverse natural soil and pond Pseudomonas communities

Summary

Introduction

All social organisms experience dilemmas between cooperators performing group-beneficial actions and cheats selfishly exploiting these actions. While highly influential as a general proof of social evolution theory, a key open question is whether cheating and the public-goods dilemma occur in natural microbial communities[8,9,10]. The most comprehensive evolutionary study on siderophore-mediated interactions used a combination of whole-genome sequencing and phenotype screening to show that many marine Vibrio strains have lost the siderophore-synthesis cluster, but kept the receptor for uptake[26] While this genomic pattern is compatible with the idea of siderophore non-producers being cheats, a direct demonstration of cheating during one-to-one strain competition is missing. We build on the work by Cordero et al.26and demonstrate that: (a) pyoverdine non-producers co-occur with producers in soil and freshwater communities of Pseudomonas; (b) non-producers can exploit siderophores of certain community a

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