Trophic interactions induce spatial self-organization of microbial consortia on rough surfaces

Wang, Gang; Or, Dani

doi:10.1038/srep06757

Cited by 23 publications

(42 citation statements)

References 44 publications

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“…However, our results demonstrate how trophic dependencies are a determining component of microbial self-organizing processes. In addition to trophic dependencies, we pointed out the roles of cell distribution in space and hydration conditions in controlling self-assembly of mutualistic consortium confirming theoretical predictions12. This is of high relevance in unsaturated soils, where average distances between microbial foci can be high and liquid connectivity relatively low.…”

Section: Discussionsupporting

confidence: 80%

Cooperation in carbon source degradation shapes spatial self-organization of microbial consortia on hydrated surfaces

Tecon

2017

Sci Rep

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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.

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Section: Discussionsupporting

confidence: 80%

Cooperation in carbon source degradation shapes spatial self-organization of microbial consortia on hydrated surfaces

Tecon

2017

Sci Rep

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“…The resulting growth conditions in soil may vary in space and time giving rise to episodic anoxic hotspots where much of the anaerobic microbial processes (e.g., denitrification) take place (Flühler et al ., ; Groffman et al ., ; Eilers et al ., ; Kuzyakov & Blagodatskaya, ). Evidence suggests that even at the aggregate‐scale microbial community structure and self‐organization may vary considerably within an aggregate and along the soil profile (Nunan et al ., ; Wang & Or, ).…”

Section: Introductionmentioning

confidence: 99%

Microbial community dynamics in soil aggregates shape biogeochemical gas fluxes from soil profiles – upscaling an aggregate biophysical model

Ebrahimi

2016

Global Change Biology

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Microbial communities inhabiting soil aggregates dynamically adjust their activity and composition in response to variations in hydration and other external conditions. These rapid dynamics shape signatures of biogeochemical activity and gas fluxes emitted from soil profiles. Recent mechanistic models of microbial processes in unsaturated aggregate-like pore networks revealed a highly dynamic interplay between oxic and anoxic microsites jointly shaped by hydration conditions and by aerobic and anaerobic microbial community abundance and self-organization. The spatial extent of anoxic niches (hotspots) flicker in time (hot moments) and support substantial anaerobic microbial activity even in aerated soil profiles. We employed an individual-based model for microbial community life in soil aggregate assemblies represented by 3D angular pore networks. Model aggregates of different sizes were subjected to variable water, carbon and oxygen contents that varied with soil depth as boundary conditions. The study integrates microbial activity within aggregates of different sizes and soil depth to obtain estimates of biogeochemical fluxes from the soil profile. The results quantify impacts of dynamic shifts in microbial community composition on CO2 and N2 O production rates in soil profiles in good agreement with experimental data. Aggregate size distribution and the shape of resource profiles in a soil determine how hydration dynamics shape denitrification and carbon utilization rates. Results from the mechanistic model for microbial activity in aggregates of different sizes were used to derive parameters for analytical representation of soil biogeochemical processes across large scales of practical interest for hydrological and climate models.

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“…For simplicity, we consider an idealized soil aggregate as the basic modeling building blocks, where details of microbial self‐organization and community functioning are simplified and parameterized based on results compiled from detailed pore‐scale model (Ebrahimi & Or, , ;). In essence, we have consolidated information from a numerical model that explicitly represents microbial life in soil pore networks considering individual cell activity (e.g., dispersion, nutrient uptake, growth, division, and death) across a range of conditions that we varied systematically (Borer et al, ; Ebrahimi & Or, ; Kim & Or, ; Wang & Or, ). The results were used to derive aggregate microbial functions that are used as inputs into an analytical aggregate model.…”

Section: Theoretical Considerationsmentioning

confidence: 99%

On Upscaling of Soil Microbial Processes and Biogeochemical Fluxes From Aggregates to Landscapes

Ebrahimi

2018

JGR Biogeosciences

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Soil microbial communities respond to spatial and temporal variations in environmental conditions (e.g., saturation and ambient temperatures) as reflected in the dynamics of microbially produced greenhouse gas (GHG) fluxes (primarily CO2, N2O, and CH4) emitted from soil surfaces. Despite considerable progress in resolving key soil microbial processes, their quantification remains largely empirical with limited predictability. We report a mechanistic and analytical modeling framework for integrating local environmental effects on GHG‐producing microbial processes primarily in soil aggregates (or other hot spots) and the upscaling of these to regional GHG fluxes. The mechanistic model enables systematic evaluation of how soil structural features (e.g., aggregation and layers), spatial variability, and dynamic ambient conditions (e.g., temperature and hydration) affect soil microbial functioning. The upscaling of microbial processes from aggregates of different sizes to soil profiles and landscapes implements mechanistically derived microbial response functions with spatial information on soil type, land cover, and resource distribution. The modeling framework was evaluated using reported field data for seasonal N2O emissions from subarctic regions resulting in reasonable agreement. The proposed analytical framework offers a practical compromise balancing a simplified representation of dynamic microbial processes that respond to local conditions with an upscalable representation of soil GHG fluxes over landscapes under changing environmental conditions.

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Trophic interactions induce spatial self-organization of microbial consortia on rough surfaces

Cited by 23 publications

References 44 publications

Cooperation in carbon source degradation shapes spatial self-organization of microbial consortia on hydrated surfaces

Cooperation in carbon source degradation shapes spatial self-organization of microbial consortia on hydrated surfaces

Microbial community dynamics in soil aggregates shape biogeochemical gas fluxes from soil profiles – upscaling an aggregate biophysical model

On Upscaling of Soil Microbial Processes and Biogeochemical Fluxes From Aggregates to Landscapes

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