Abstract

Mounting evidence suggests that natural microbial communities exhibit a high level of spatial organization at the micrometric scale that facilitate ecological interactions and support biogeochemical cycles. Microbial patterns are difficult to study definitively in natural environments due to complex biodiversity, observability and variable physicochemical factors. Here, we examine how trophic dependencies give rise to self-organized spatial patterns of a well-defined bacterial consortium grown on hydrated surfaces. The model consortium consisted of two Pseudomonas putida mutant strains that can fully degrade the aromatic hydrocarbon toluene. We demonstrated that obligate cooperation in toluene degradation (cooperative mutualism) favored convergence of 1:1 partner ratio and strong intermixing at the microscale (10–100 μm). In contrast, competition for benzoate, a compound degraded independently by both strains, led to distinct segregation patterns. Emergence of a persistent spatial pattern has been predicted for surface attached microbial activity in liquid films that mediate diffusive exchanges while permitting limited cell movement (colony expansion). This study of a simple microbial consortium offers mechanistic glimpses into the rules governing the assembly and functioning of complex sessile communities, and points to general principles of spatial organization with potential applications for natural and engineered microbial systems.

Highlights

  • Mounting evidence suggests that natural microbial communities exhibit a high level of spatial organization at the micrometric scale that facilitate ecological interactions and support biogeochemical cycles

  • The consortium strains derived from Pseudomonas putida F1 (PpF1), a soil bacterium which can use the hydrocarbon toluene as sole carbon and energy source[31]

  • We have shown that, when paired and in presence of toluene, the complementary strains P. putida F4 (PpF4) and P. putida F107 (PpF107) acted as a cross-feeding consortium, reinstating the PpF1 phenotype on solid and in liquid media (Fig. 1b,c)

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Summary

Introduction

Mounting evidence suggests that natural microbial communities exhibit a high level of spatial organization at the micrometric scale that facilitate ecological interactions and support biogeochemical cycles. The study of microbial spatial patterns in soil, is inherently difficult due to the phylogenetic complexity of communities, uncontrolled dynamic conditions, observational constraints of opaque soil components, and experimental sampling scales that are often larger than the scales of trophic interactions. For these reasons, and despite the ubiquity and apparent importance of microbial sessile structures in most environments, our understanding of the mechanisms governing the spatial assembly and functioning of consortia remains limited. The study demonstrated how different types of trophic interactions and physicochemical factors give rise to formation of functional spatial patterns relevant to microbial ecology in complex environmental systems

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