Exometabolite niche partitioning among sympatric soil bacteria.

Richard Baran,Eric Hummel,Hinsby Cadillo-Quiroz,Benjamin P Bowen,Ulas Karaoz,Romy Chakraborty,Ferran Garcia-Pichel,Ulisses Nunes Da Rocha,Eoin L Brodie,Jazmine Mayberry-Lewis,Trent R Northen

doi:10.1038/ncomms9289

Abstract

Soils are arguably the most microbially diverse ecosystems. Physicochemical properties have been associated with the maintenance of this diversity. Yet, the role of microbial substrate specialization is largely unexplored since substrate utilization studies have focused on simple substrates, not the complex mixtures representative of the soil environment. Here we examine the exometabolite composition of desert biological soil crusts (biocrusts) and the substrate preferences of seven biocrust isolates. The biocrust's main primary producer releases a diverse array of metabolites, and isolates of physically associated taxa use unique subsets of the complex metabolite pool. Individual isolates use only 13−26% of available metabolites, with only 2 out of 470 used by all and 40% not used by any. An extension of this approach to a mesophilic soil environment also reveals high levels of microbial substrate specialization. These results suggest that exometabolite niche partitioning may be an important factor in the maintenance of microbial diversity.

Highlights

Soils are arguably the most microbially diverse ecosystems
Related studies on microbial growth have suggested that isolates on copiotrophic media have narrower substrate preferences than those obtained on oligotrophic media[22] and that growth depends both on the specific metabolites present in their environment and on their concentrations[23,24]
Unlike these early studies that have focused on single substrate utilization, technological advances in exometabolomics[25] enable characterization of microbial metabolite utilization from mixtures of hundreds of metabolites with relevant composition and concentrations for a particular environment of interest

Summary

Introduction

Soils are arguably the most microbially diverse ecosystems. Physicochemical properties have been associated with the maintenance of this diversity. Exometabolomics has the potential to delineate microbial exometabolite niches[25,27] for cooccurring (sympatric) bacteria based on observed specialized and preferential use of specific metabolites from the exometabolite pool (Fig. 1), helping couple soil metabolite composition to microbial diversity, and improve our understanding of soil trophic webs and nutrient cycling[28] This interrogation of the extent of microbial utilization from relevant substrate mixtures addresses limitations associated with the single substrate utilization patterns[22] and enables the examination of the utilization of novel or unexpected metabolites—such as the utilization of ergothioneine by Shewanella oneidensis[29]. This may be relevant to uncultured microorganisms, where dependence on novel metabolites and multiple substrates may be the rule not the exception[30,31] under low nutrient conditions[32]

Methods

Results

Conclusion